Functional traits of fossil plants.

A minuscule fraction of the Earth's paleobiological diversity is preserved in the geological record as fossils. What plant remnants have withstood taphonomic filtering, fragmentation, and alteration in their journey to become part of the fossil record provide unique information on how plants functioned in paleo-ecosystems through their traits. Plant traits are measurable morphological, anatomical, physiological, biochemical, or phenological characteristics that potentially affect their environment and fitness. Here, we review the rich literature of paleobotany, through the lens of contemporary trait-based ecology, to evaluate which well-established extant plant traits hold the greatest promise for application to fossils. In particular, we focus on fossil plant functional traits, those measurable properties of leaf, stem, reproductive, or whole plant fossils that offer insights into the functioning of the plant when alive. The limitations of a trait-based approach in paleobotany are considerable. However, in our critical assessment of over 30 extant traits we present an initial, semi-quantitative ranking of 26 paleo-functional traits based on taphonomic and methodological criteria on the potential of those traits to impact Earth system processes, and for that impact to be quantifiable. We demonstrate how valuable inferences on paleo-ecosystem processes (pollination biology, herbivory), past nutrient cycles, paleobiogeography, paleo-demography (life history), and Earth system history can be derived through the application of paleo-functional traits to fossil plants.

Nitrogen isotopes reveal independent origins of N2-fixing symbiosis in extant cycad lineages.

Cycads are ancient seed plants (gymnosperms) that emerged by the early Permian. Although they were common understory flora and food for dinosaurs in the Mesozoic, their abundance declined markedly in the Cenozoic. Extant cycads persist in restricted populations in tropical and subtropical habitats and, with their conserved morphology, are often called 'living fossils.' All surviving taxa receive nitrogen from symbiotic N2-fixing cyanobacteria living in modified roots, suggesting an ancestral origin of this symbiosis. However, such an ancient acquisition is discordant with the abundance of cycads in Mesozoic fossil assemblages, as modern N2-fixing symbioses typically occur only in nutrient-poor habitats where advantageous for survival. Here, we use foliar nitrogen isotope ratios-a proxy for N2 fixation in modern plants-to probe the antiquity of the cycad-cyanobacterial symbiosis. We find that fossilized cycad leaves from two Cenozoic representatives of extant genera have nitrogen isotopic compositions consistent with microbial N2 fixation. In contrast, all extinct cycad genera have nitrogen isotope ratios that are indistinguishable from co-existing non-cycad plants and generally inconsistent with microbial N2 fixation, pointing to nitrogen assimilation from soils and not through symbiosis. This pattern indicates that, rather than being ancestral within cycads, N2-fixing symbiosis arose independently in the lineages leading to living cycads during or after the Jurassic. The preferential survival of these lineages may therefore reflect the effects of competition with angiosperms and Cenozoic climatic change.

Toward a Cenozoic history of atmospheric CO2.

The geological record encodes the relationship between climate and atmospheric carbon dioxide (CO2) over long and short timescales, as well as potential drivers of evolutionary transitions. However, reconstructing CO2 beyond direct measurements requires the use of paleoproxies and herein lies the challenge, as proxies differ in their assumptions, degree of understanding, and even reconstructed values. In this study, we critically evaluated, categorized, and integrated available proxies to create a high-fidelity and transparently constructed atmospheric CO2 record spanning the past 66 million years. This newly constructed record provides clearer evidence for higher Earth system sensitivity in the past and for the role of CO2 thresholds in biological and cryosphere evolution.

CO2 -induced biochemical changes in leaf volatiles decreased fire-intensity in the run-up to the Triassic-Jurassic boundary.

The Triassic-Jurassic boundary marks the third largest mass extinction event in the Phanerozoic, characterized by a rise in CO2 -concentrations from c. 600 ppm to c. 2100-2400 ppm, coupled with a c. 3.0-4.0°C temperature rise. This is hypothesized to have induced major floral turnover, altering vegetation structure, composition and leaf morphology, which in turn are hypothesized to have driven changes in wildfire. However, the effects of elevated CO2 on fuel properties, such as chemical composition of leaves, are also important in influencing fire behaviour, but yet have not been considered. We test this by selecting three Triassic analogue species grown experimentally in different atmospheric compositions, and analyse variations in leaf chemistry, and leaf level flammability. These data were used to inform a fire behaviour model. We find that all three species tested showed a reduction in their volatile component, leading to lower flammability. Accounting for these variations in a model, our results suggest that leaf intrinsic flammability has a measurable impact on modelled fire behaviour. If scaled up to ecosystem level, periods of elevated CO2 may therefore be capable of inducing both biochemical and morphological changes in fuel properties, and thus may be capable of influencing fire behaviour.

Freeze tolerance influenced forest cover and hydrology during the Pennsylvanian.

The distribution of forest cover alters Earth surface mass and energy exchange and is controlled by physiology, which determines plant environmental limits. Ancient plant physiology, therefore, likely affected vegetation-climate feedbacks. We combine climate modeling and ecosystem-process modeling to simulate arboreal vegetation in the late Paleozoic ice age. Using GENESIS V3 global climate model simulations, varying pCO2, pO2, and ice extent for the Pennsylvanian, and fossil-derived leaf C:N, maximum stomatal conductance, and specific conductivity for several major Carboniferous plant groups, we simulated global ecosystem processes at a 2° resolution with Paleo-BGC. Based on leaf water constraints, Pangaea could have supported widespread arboreal plant growth and forest cover. However, these models do not account for the impacts of freezing on plants. According to our interpretation, freezing would have affected plants in 59% of unglaciated land during peak glacial periods and 73% during interglacials, when more high-latitude land was unglaciated. Comparing forest cover, minimum temperatures, and paleo-locations of Pennsylvanian-aged plant fossils from the Paleobiology Database supports restriction of forest extent due to freezing. Many genera were limited to unglaciated land where temperatures remained above -4 °C. Freeze-intolerance of Pennsylvanian arboreal vegetation had the potential to alter surface runoff, silicate weathering, CO2 levels, and climate forcing. As a bounding case, we assume total plant mortality at -4 °C and estimate that contracting forest cover increased net global surface runoff by up to 6.1%. Repeated freezing likely influenced freeze- and drought-tolerance evolution in lineages like the coniferophytes, which became increasingly dominant in the Permian and early Mesozoic.

Enhancing the productivity of ryegrass at elevated CO2 is dependent on tillering and leaf area development rather than leaf-level photosynthesis.

Whilst a range of strategies have been proposed for enhancing crop productivity, many recent studies have focused primarily on enhancing leaf photosynthesis under current atmospheric CO2 concentrations. Given that the atmospheric CO2 concentration is likely to increase significantly in the foreseeable future, an alternative/complementary strategy might be to exploit any variability in the enhancement of growth/yield and photosynthesis at higher CO2 concentrations. To explore this, we investigated the responses of a diverse range of wild and cultivated ryegrass genotypes, with contrasting geographical origins, to ambient and elevated CO2 concentrations and examined what genetically tractable plant trait(s) might be targeted by plant breeders for future yield enhancements. We found substantial ~7-fold intraspecific variations in biomass productivity among the different genotypes at both CO2 levels, which were related primarily to differences in tillering/leaf area, with only small differences due to leaf photosynthesis. Interestingly, the ranking of genotypes in terms of their response to both CO2 concentrations was similar. However, as expected, estimates of whole-plant photosynthesis were strongly correlated with plant productivity. Our results suggest that greater yield gains under elevated CO2 are likely through the exploitation of genetic differences in tillering and leaf area rather than focusing solely on improving leaf photosynthesis.

Past climates inform our future.

As the world warms, there is a profound need to improve projections of climate change. Although the latest Earth system models offer an unprecedented number of features, fundamental uncertainties continue to cloud our view of the future. Past climates provide the only opportunity to observe how the Earth system responds to high carbon dioxide, underlining a fundamental role for paleoclimatology in constraining future climate change. Here, we review the relevancy of paleoclimate information for climate prediction and discuss the prospects for emerging methodologies to further insights gained from past climates. Advances in proxy methods and interpretations pave the way for the use of past climates for model evaluation-a practice that we argue should be widely adopted.

Carboniferous plant physiology breaks the mold.

How plants have shaped Earth surface feedbacks over geologic time is a key question in botanical and geological inquiry. Recent work has suggested that biomes during the Carboniferous Period contained plants with extraordinary physiological capacity to shape their environment, contradicting the previously dominant view that plants only began to actively moderate the Earth's surface with the rise of angiosperms during the Mesozoic Era. A recently published Viewpoint disputes this recent work, thus here, we document in detail, the mechanistic underpinnings of our modeling and illustrate the extraordinary ecophysiological nature of Carboniferous plants.

Rising CO2 drives divergence in water use efficiency of evergreen and deciduous plants.

Intrinsic water use efficiency (iWUE), defined as the ratio of photosynthesis to stomatal conductance, is a key variable in plant physiology and ecology. Yet, how rising atmospheric CO2 concentration affects iWUE at broad species and ecosystem scales is poorly understood. In a field-based study of 244 woody angiosperm species across eight biomes over the past 25 years of increasing atmospheric CO2 (~45 ppm), we show that iWUE in evergreen species has increased more rapidly than in deciduous species. Specifically, the difference in iWUE gain between evergreen and deciduous taxa diverges along a mean annual temperature gradient from tropical to boreal forests and follows similar observed trends in leaf functional traits such as leaf mass per area. Synthesis of multiple lines of evidence supports our findings. This study provides timely insights into the impact of Anthropocene climate change on forest ecosystems and will aid the development of next-generation trait-based vegetation models.

A Novel Hypothesis for the Role of Photosynthetic Physiology in Shaping Macroevolutionary Patterns.

The fossil record and models of atmospheric concentrations of O2 and CO2 suggest that past shifts in plant ecological dominance often coincided with dramatic changes in Earth's atmospheric composition. This study tested the effects of past changes in atmospheric composition on the photosynthetic physiology of a limited range of early-diverging angiosperms (eight), gymnosperms (three), and ferns (two). We performed physiological measurements on all species and used the results to parameterize simulations of their photosynthetic paleophysiology using three independent modeling approaches. Unique physiological attributes were identified for the three evolutionary groups: angiosperm taxa displayed significantly higher mesophyll conductance (g m), yet their stomatal conductance (g s) was lower than that of ferns. Gymnosperm taxa displayed low g s and g m, but they partially offset their significant diffusional limitations on photosynthesis through their higher maximum Rubisco carboxylation rate. Despite their high total conductance to CO2, fern taxa lacked an optimized control of g s, which was reflected in their low intrinsic water use efficiency. Simulations of the photosynthetic physiology of ferns, angiosperms, and gymnosperms through Earth's history demonstrated that past fluctuations in O2 and CO2 concentrations may have resulted in significant shifts in the relative competitiveness of the three evolutionary groups. Although preliminary because of limited species sampling, these findings hint at a potential mechanistic basis for the observed broad temporal correlation between atmospheric change and shifts in plant evolutionary group-level richness observed in the fossil record and are presented as a framework to be tested with paleophotosynthetic proxies and through increased species sampling.

Convergence in Maximum Stomatal Conductance of C3 Woody Angiosperms in Natural Ecosystems Across Bioclimatic Zones.

Stomatal conductance (g s) in terrestrial vegetation regulates the uptake of atmospheric carbon dioxide for photosynthesis and water loss through transpiration, closely linking the biosphere and atmosphere and influencing climate. Yet, the range and pattern of g s in plants from natural ecosystems across broad geographic, climatic, and taxonomic ranges remains poorly quantified. Furthermore, attempts to characterize g s on such scales have predominantly relied upon meta-analyses compiling data from many different studies. This approach may be inherently problematic as it combines data collected using unstandardized protocols, sometimes over decadal time spans, and from different habitat groups. Using a standardized protocol, we measured leaf-level g s using porometry in 218 C3 woody angiosperm species in natural ecosystems representing seven bioclimatic zones. The resulting dataset of 4273 g s measurements, which we call STraits (Stomatal Traits), was used to determine patterns in maximum g s (g smax) across bioclimatic zones and whether there was similarity in the mean g smax of C3 woody angiosperms across ecosystem types. We also tested for differential g smax in two broadly defined habitat groups - open-canopy and understory-subcanopy - within and across bioclimatic zones. We found strong convergence in mean g smax of C3 woody angiosperms in the understory-subcanopy habitats across six bioclimatic zones, but not in open-canopy habitats. Mean g smax in open-canopy habitats (266 ± 100 mmol m-2 s-1) was significantly higher than in understory-subcanopy habitats (233 ± 86 mmol m-2 s-1). There was also a central tendency in the overall dataset to operate toward a g smax of ∼250 mmol m-2 s-1. We suggest that the observed convergence in mean g smax of C3 woody angiosperms in the understory-subcanopy is due to a buffering of g smax against macroclimate effects which will lead to differential response of C3 woody angiosperm vegetation in these two habitats to future global change. Therefore, it will be important for future studies of g smax to categorize vegetation according to habitat group.

Higher species richness enhances yield stability in intensively managed grasslands with experimental disturbance.

Climate models predict increased frequency and severity of drought events. At an Irish and Swiss site, experimental summer droughts were applied over two successive years to grassland plots sown with one, two or four grassland species with contrasting functional traits. Mean yield and plot-to-plot variance of yield were measured across harvests during drought and after a subsequent post-drought recovery period. At both sites, there was a positive relationship between species richness and yield. Under rainfed control conditions, mean yields of four-species communities were 32% (Wexford, Ireland) and 51% (Zürich, Switzerland) higher than in monocultures. This positive relationship was also evident under drought, despite significant average yield reductions (-27% at Wexford; -21% at Zürich). Four-species communities had lower plot-to-plot variance of yield compared to monoculture or two-species communities under both rainfed and drought conditions, which demonstrates higher yield stability in four-species communities. At the Swiss but not the Irish site, a high degree of species asynchrony could be identified as a mechanism underlying increased temporal stability in four-species communities. These results indicate the high potential of multi-species grasslands as an adaptation strategy against drought events and help achieve sustainable intensification under both unperturbed and perturbed environmental conditions.

Paleobotany and Global Change: Important Lessons for Species to Biomes from Vegetation Responses to Past Global Change.

Human carbon use during the next century will lead to atmospheric carbon dioxide concentrations (pCO2) that have been unprecedented for the past 50-100+ million years according to fossil plant-based CO2 estimates. The paleobotanical record of plants offers key insights into vegetation responses to past global change, including suitable analogs for Earth's climatic future. Past global warming events have resulted in transient poleward migration at rates that are equivalent to the lowest climate velocities required for current taxa to keep pace with climate change. Paleobiome reconstructions suggest that the current tundra biome is the biome most threatened by global warming. The common occurrence of paleoforests at high polar latitudes when pCO2 was above 500 ppm suggests that the advance of woody shrub and tree taxa into tundra environments may be inevitable. Fossil pollen studies demonstrate the resilience of wet tropical forests to global change up to 700 ppm CO2, contrary to modeled predictions of the future. The paleobotanical record also demonstrates a high capacity for functional trait evolution as an additional strategy to migration and maintenance of a species' climate envelope in response to global change.

Dynamic Carboniferous tropical forests: new views of plant function and potential for physiological forcing of climate.

Contents 1333 I. 1334 II. 1335 III. 1339 IV. 1344 V. 1347 VI. 1347 1348 1348 References 1348 SUMMARY: The Carboniferous, the time of Earth's penultimate icehouse and widespread coal formation, was dominated by extinct lineages of early-diverging vascular plants. Studies of nearest living relatives of key Carboniferous plants suggest that their physiologies and growth forms differed substantially from most types of modern vegetation, particularly forests. It remains a matter of debate precisely how differently and to what degree these long-extinct plants influenced the environment. Integrating biophysical analysis of stomatal and vascular conductivity with geochemical analysis of fossilized tissues and process-based ecosystem-scale modeling yields a dynamic and unique perspective on these paleoforests. This integrated approach indicates that key Carboniferous plants were capable of growth and transpiration rates that approach values found in extant crown-group angiosperms, differing greatly from comparatively modest rates found in their closest living relatives. Ecosystem modeling suggests that divergent stomatal conductance, leaf sizes and stem life span between dominant clades would have shifted the balance of soil-atmosphere water fluxes, and thus surface runoff flux, during repeated, climate-driven, vegetation turnovers. This synthesis highlights the importance of 'whole plant' physiological reconstruction of extinct plants and the potential of vascular plants to have influenced the Earth system hundreds of millions of years ago through vegetation-climate feedbacks.

Co-ordination in Morphological Leaf Traits of Early Diverging Angiosperms Is Maintained Following Exposure to Experimental Palaeo-atmospheric Conditions of Sub-ambient O2 and Elevated CO2.

In order to be successful in a given environment a plant should invest in a vein network and stomatal distribution that ensures balance between both water supply and demand. Vein density (Dv) and stomatal density (SD) have been shown to be strongly positively correlated in response to a range of environmental variables in more recently evolved plant species, but the extent of this relationship has not been confirmed in earlier diverging plant lineages. In order to examine the effect of a changing atmosphere on the relationship between Dv and SD, five early-diverging plant species representing two different reproductive plant grades were grown for 7 months in a palaeo-treatment comprising an O2:CO2 ratio that has occurred multiple times throughout plant evolutionary history. Results show a range of species-specific Dv and SD responses to the palaeo-treatment, however, we show that the strong relationship between Dv and SD under modern ambient atmospheric composition is maintained following exposure to the palaeo-treatment. This suggests strong inter-specific co-ordination between vein and stomatal traits for our study species even under relatively extreme environmental change. This co-ordination supports existing plant function proxies that use the distance between vein endings and stomata (Dm) to infer plant palaeo-physiology.

Does Size Matter? Atmospheric CO2 May Be a Stronger Driver of Stomatal Closing Rate Than Stomatal Size in Taxa That Diversified under Low CO2.

One strategy for plants to optimize stomatal function is to open and close their stomata quickly in response to environmental signals. It is generally assumed that small stomata can alter aperture faster than large stomata. We tested the hypothesis that species with small stomata close faster than species with larger stomata in response to darkness by comparing rate of stomatal closure across an evolutionary range of species including ferns, cycads, conifers, and angiosperms under controlled ambient conditions (380 ppm CO2; 20.9% O2). The two species with fastest half-closure time and the two species with slowest half-closure time had large stomata while the remaining three species had small stomata, implying that closing rate was not correlated with stomatal size in these species. Neither was response time correlated with stomatal density, phylogeny, functional group, or life strategy. Our results suggest that past atmospheric CO2 concentration during time of taxa diversification may influence stomatal response time. We show that species which last diversified under low or declining atmospheric CO2 concentration close stomata faster than species that last diversified in a high CO2 world. Low atmospheric [CO2] during taxa diversification may have placed a selection pressure on plants to accelerate stomatal closing to maintain adequate internal CO2 and optimize water use efficiency.

Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution.

Understanding the drivers of geological-scale patterns in plant macroevolution is limited by a hesitancy to use measurable traits of fossils to infer palaeoecophysiological function. Here, scaling relationships between morphological traits including maximum theoretical stomatal conductance (gmax ) and leaf vein density (Dv ) and physiological measurements including operational stomatal conductance (gop ), saturated (Asat ) and maximum (Amax ) assimilation rates were investigated for 18 extant taxa in order to improve understanding of angiosperm diversification in the Cretaceous. Our study demonstrated significant relationships between gop , gmax and Dv that together can be used to estimate gas exchange and the photosynthetic capacities of fossils. We showed that acquisition of high gmax in angiosperms conferred a competitive advantage over gymnosperms by increasing the dynamic range (plasticity) of their gas exchange and expanding their ecophysiological niche space. We suggest that species with a high gmax (> 1400 mmol m(-2) s(-1) ) would have been capable of maintaining a high Amax as the atmospheric CO2 declined through the Cretaceous, whereas gymnosperms with a low gmax would experience severe photosynthetic penalty. Expansion of the ecophysiological niche space in angiosperms, afforded by coordinated evolution of high gmax , Dv and increased plasticity in gop , adds further functional insights into the mechanisms driving angiosperm speciation.