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.

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.

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.

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.

The prevalence of pre-operative anaemia and an examination of its effect on transfusion practice between sexes: A multicentre retrospective study.

Pre-operative anaemia affects one third of patients presenting for surgery and is associated with increased peri-operative morbidity and mortality. Most studies on this subject make a distinction in acceptable haemoglobin level between sexes. We analysed data for patients undergoing major elective surgery, with pre-operative anaemia defined as haemoglobin <13 g/dL. Data was collected for 1074 patients, of whom 411 (38.3%) had pre-operative anaemia. The odds of red cell transfusion were significantly higher in patients with pre-operative anaemia, OR = 4.35 [95%CI OR: 3.0- 6.2]. Additional binary logistic regression results identified haemoglobin level, male gender and increasing age as independent predictors for red cell transfusion. The length of post-operative stay was also significantly higher in anaemic patients, those with lower haemoglobin, males and older patients. Women were twice as likely to have a haemoglobin < 13 g/dl as men. Women were also 3.55 times more likely not to be transfused despite being anaemic. This suggests differences in clinician's attitudes to transfusion limits in women, despite Blaudszun et al. 2018 showing that women with borderline anaemia (Hb 12-12.9 g/dL) are: more likely to be transfused; to be transfused more units of red cells; and to have longer lengths of hospital stay than non- anaemic women. A change in attitude to acceptable haemoglobin in women is needed. Increased clinician awareness of the associated morbidity of even a mild reduction in haemoglobin in women is required to result in more pro-active anaemia management pre-operatively and less allogenic red cell transfusion, shorter lengths of hospital stay and overall decreased morbidity.

Plant responses to decadal scale increments in atmospheric CO2 concentration: comparing two stomatal conductance sampling methods.

MAIN CONCLUSION: Our study demonstrated that the species respond non-linearly to increases in CO2 concentration when exposed to decadal changes in CO2, representing the year 1987, 2025, 2051, and 2070, respectively. There are several lines of evidence suggesting that the vast majority of C3 plants respond to elevated atmospheric CO2 by decreasing their stomatal conductance (gs). However, in the majority of CO2 enrichment studies, the response to elevated CO2 are tested between plants grown under ambient (380-420 ppm) and high (538-680 ppm) CO2 concentrations and measured usually at single time points in a diurnal cycle. We investigated gs responses to simulated decadal increments in CO2 predicted over the next 4 decades and tested how measurements of gs may differ when two alternative sampling methods are employed (infrared gas analyzer [IRGA] vs. leaf porometer). We exposed Populus tremula, Popolus tremuloides and Sambucus racemosa to four different CO2 concentrations over 126 days in experimental growth chambers at 350, 420, 490 and 560 ppm CO2; representing the years 1987, 2025, 2051, and 2070, respectively (RCP4.5 scenario). Our study demonstrated that the species respond non-linearly to increases in CO2 concentration when exposed to decadal changes in CO2. Under natural conditions, maximum operational gs is often reached in the late morning to early afternoon, with a mid-day depression around noon. However, we showed that the daily maximum gs can, in some species, shift later into the day when plants are exposed to only small increases (70 ppm) in CO2. A non-linear decreases in gs and a shifting diurnal stomatal behavior under elevated CO2, could affect the long-term daily water and carbon budget of many plants in the future, and therefore alter soil-plant-atmospheric processes.

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.

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.

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.

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.

Genome-wide transcriptomic analysis of the effects of sub-ambient atmospheric oxygen and elevated atmospheric carbon dioxide levels on gametophytes of the moss, Physcomitrella patens.

It is widely accepted that atmospheric O2 has played a key role in the development of life on Earth, as evident from the coincidence between the rise of atmospheric O2 concentrations in the Precambrian and biological evolution. Additionally, it has also been suggested that low atmospheric O2 is one of the major drivers for at least two of the five mass-extinction events in the Phanerozoic. At the molecular level, our understanding of the responses of plants to sub-ambient O2 concentrations is largely confined to studies of the responses of underground organs, e.g. roots to hypoxic conditions. Oxygen deprivation often results in elevated CO2 levels, particularly under waterlogged conditions, due to slower gas diffusion in water compared to air. In this study, changes in the transcriptome of gametophytes of the moss Physcomitrella patens arising from exposure to sub-ambient O2 of 13% (oxygen deprivation) and elevated CO2 (1500 ppmV) were examined to further our understanding of the responses of lower plants to changes in atmospheric gaseous composition. Microarray analyses revealed that the expression of a large number of genes was affected under elevated CO2 (814 genes) and sub-ambient O2 conditions (576 genes). Intriguingly, the expression of comparatively fewer numbers of genes (411 genes) was affected under a combination of both sub-ambient O2 and elevated CO2 condition (low O2-high CO2). Overall, the results point towards the effects of atmospheric changes in CO2 and O2 on transcriptional reprogramming, photosynthetic regulation, carbon metabolism, and stress responses.

The severity of wheat diseases increases when plants and pathogens are acclimatized to elevated carbon dioxide.

Wheat diseases present a constant and evolving threat to food security. We have little understanding as to how increased atmospheric carbon dioxide levels will affect wheat diseases and thus the security of grain supply. Atmospheric CO2 exceeded the 400 ppmv benchmark in 2013 and is predicted to double or even treble by the end of the century. This study investigated the impact of both pathogen and wheat acclimation to elevated CO2 on the development of Fusarium head blight (FHB) and Septoria tritici blotch (STB) disease of wheat. Here, plants and pathogens were cultivated under either 390 or 780 ppmv CO2 for a period (two wheat generations, multiple pathogen subcultures) prior to standard disease trials. Acclimation of pathogens and the wheat cultivar Remus to elevated CO2 increased the severity of both STB and FHB diseases, relative to ambient conditions. The effect of CO2 on disease development was greater for FHB than for STB. The highest FHB disease levels and associated yield losses were recorded for elevated CO2 -acclimated pathogen on elevated CO2 -acclimated wheat. When similar FHB experiments were conducted using the disease-resistant cultivar CM82036, pathogen acclimation significantly enhanced disease levels and yield loss under elevated CO2 conditions, thereby indicating a reduction in the effectiveness of the defence pathways innate to this wheat cultivar. We conclude that acclimation to elevated CO2 over the coming decades will have a significant influence on the outcome of plant-pathogen interactions and the durability of disease resistance.

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.

New methods reveal oldest known fossil epiphyllous moss: Bryiidites utahensis gen. et sp. nov. (Bryidae).

PREMISE OF THE STUDY: Epiphyllous bryophytes are a highly characteristic feature of many humid tropical forest ecosystems. In contrast to the extensive fossil record for the leaves of their host plants, the record is virtually nonexistent for the epiphylls themselves, despite a fossil record for mosses that begins in the Middle Carboniferous Period, 330 million years ago. METHODS: Epifluorescence optical microscopy, scanning electron microscopy, and atomic force microscopy were employed to investigate an intimate association between a newly discovered epiphyllous moss and a Lauraceae plant host from the middle Cretaceous. KEY RESULTS: We describe the oldest fossil specimen of an epiphyllous moss, Bryiidites utahensis gen. et sp. nov., identified from an individual specimen only 450 µm long, situated on an approximately one millimeter square fossil leaf fragment. The moss epiphyll is exquisitely preserved as germinating spores and short-celled protonemata with transverse and oblique cross-walls closely matching those of extant epiphyllous mosses on the surface of the plant-leaf hosts. CONCLUSIONS: The extension of the epiphyll record back to the middle Cretaceous provides fossil evidence for the appearance of epiphyllous mosses during the diversification of flowering plants, at least 95 million years ago. It also provides substantive evidence for a tropical maritime climate in central North America during the middle Cretaceous.

Co-ordination of physiological and morphological responses of stomata to elevated [CO2] in vascular plants.

Plant stomata display a wide range of short-term behavioural and long-term morphological responses to atmospheric carbon dioxide concentration ([CO(2)]). The diversity of responses suggests that plants may have different strategies for controlling gas exchange, yet it is not known whether these strategies are co-ordinated in some way. Here, we test the hypothesis that there is co-ordination of physiological (via aperture change) and morphological (via stomatal density change) control of gas exchange by plants. We examined the response of stomatal conductance (G(s)) to instantaneous changes in external [CO(2)] (C(a)) in an evolutionary cross-section of vascular plants grown in atmospheres of elevated [CO(2)] (1,500 ppm) and sub-ambient [O(2)] (13.0 %) compared to control conditions (380 ppm CO(2), 20.9 % O(2)). We found that active control of stomatal aperture to [CO(2)] above current ambient levels was not restricted to angiosperms, occurring in the gymnosperms Lepidozamia peroffskyana and Nageia nagi. The angiosperm species analysed appeared to possess a greater respiratory demand for stomatal movement than gymnosperm species displaying active stomatal control. Those species with little or no control of stomatal aperture (termed passive) to C(a) were more likely to exhibit a reduction in stomatal density than species with active stomatal control when grown in atmospheres of elevated [CO(2)]. The relationship between the degree of stomatal aperture control to C(a) above ambient and the extent of any reduction in stomatal density may suggest the co-ordination of physiological and morphological responses of stomata to [CO(2)] in the optimisation of water use efficiency. This trade-off between stomatal control strategies may have developed due to selective pressures exerted by the costs associated with passive and active stomatal control.

An explanation for conflicting records of Triassic-Jurassic plant diversity.

Macrofossils (mostly leaves) and sporomorphs (pollen and spores) preserve conflicting records of plant biodiversity during the end-Permian (P-Tr), Triassic-Jurassic (Tr-J), and end-Cretaceous (K-T) mass extinctions. Estimates of diversity loss based on macrofossils are typically much higher than estimates of diversity loss based on sporomorphs. Macrofossils from the Tr-J of East Greenland indicate that standing species richness declined by as much as 85% in the Late Triassic, whereas sporomorph records from the same region, and from elsewhere in Europe, reveal little evidence of such catastrophic diversity loss. To understand this major discrepancy, we have used a new high-resolution dataset of sporomorph assemblages from Astartekløft, East Greenland, to directly compare the macrofossil and sporomorph records of Tr-J plant biodiversity. Our results show that sporomorph assemblages from the Tr-J boundary interval are 10-12% less taxonomically diverse than sporomorph assemblages from the Late Triassic, and that vegetation composition changed rapidly in the boundary interval as a result of emigration and/or extirpation of taxa rather than immigration and/or origination of taxa. An analysis of the representation of different plant groups in the macrofossil and sporomorph records at Astartekløft reveals that reproductively specialized plants, including cycads, bennettites and the seed-fern Lepidopteris are almost absent from the sporomorph record. These results provide a means of reconciling the macrofossil and sporomorph records of Tr-J vegetation change, and may help to understand vegetation change during the P-Tr and K-T mass extinctions and around the Paleocene-Eocene Thermal Maximum.

Baseline intrinsic flammability of Earth's ecosystems estimated from paleoatmospheric oxygen over the past 350 million years.

Atmospheric oxygen (O(2)) is estimated to have varied greatly throughout Earth's history and has been capable of influencing wildfire activity wherever fuel and ignition sources were present. Fires consume huge quantities of biomass in all ecosystems and play an important role in biogeochemical cycles. This means that understanding the influence of O(2) on past fire activity has far-reaching consequences for the evolution of life and Earth's biodiversity over geological timescales. We have used a strong electrical ignition source to ignite smoldering fires, and we measured their self-sustaining propagation in atmospheres of different oxygen concentrations. These data have been used to build a model that we use to estimate the baseline intrinsic flammability of Earth's ecosystems according to variations in O(2) over the past 350 million years (Ma). Our aim is to highlight times in Earth's history when fire has been capable of influencing the Earth system. We reveal that fire activity would be greatly suppressed below 18.5% O(2), entirely switched off below 16% O(2), and rapidly enhanced between 19-22% O(2). We show that fire activity and, therefore, its influence on the Earth system would have been high during the Carboniferous (350-300 Ma) and Cretaceous (145-65 Ma) periods; intermediate in the Permian (299-251 Ma), Late Triassic (285-201 Ma), and Jurassic (201-145 Ma) periods; and surprisingly low to lacking in the Early-Middle Triassic period between 250-240 Ma. These baseline variations in Earth's flammability must be factored into our understanding of past vegetation, biodiversity, evolution, and biogeochemical cycles.

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.

Ancient atmospheres and the evolution of oxygen sensing via the hypoxia-inducible factor in metazoans.

Metazoan diversification occurred during a time when atmospheric oxygen levels fluctuated between 15 and 30%. The hypoxia-inducible factor (HIF) is a primary regulator of the adaptive transcriptional response to hypoxia. Although the HIF pathway is highly conserved, its complexity increased during periods when atmospheric oxygen concentrations were increasing. Thus atmospheric oxygen levels may have provided a selection force on the development of cellular oxygen-sensing pathways.