Matthew Haworth

Macroecological responses of terrestrial vegetation to climatic and atmospheric change across the Triassic/Jurassic boundary in East Greenland

Abstract The magnitude and pace of terrestrial plant extinction and macroecological change associated with the Triassic/Jurassic (Tr/J) mass extinction boundary have not been quantified using paleoecological data. However, tracking the diversity and ecology of primary producers provides an ideal surrogate with which to explore patterns of ecosystem stability, collapse, and recovery and to explicitly test for gradual versus catastrophic causal mechanisms of extinction. We present an analysis of the vegetation dynamics in the Jameson Land Basin, East Greenland, spanning the Tr/J extinction event, from a census collected paleoecological data set of 4303 fossil leaf specimens, in an attempt to better constrain our understanding of the causes and consequences of the fourth greatest extinction event in earth history. Our analyses reveal (1) regional turnover of ecological dominants between Triassic and Jurassic plant communities, (2) marked structural changes in the vegetation as reflected by potential loss of a mid-canopy habit, and (3) decline in generic-level richness and evenness and change in ecological composition prior to the Tr/J boundary; all of these findings argue against a single catastrophic causal mechanism, such as a meteorite impact for Tr/J extinctions. We identify various key ecological and biological traits that increased extinction risk at the Tr/J boundary and corroborate predictions of meta-population theory or plant ecophysiological models. These include ecological rarity, complex reproductive biology, and large leaf size. Recovery in terms of generic-level richness was quite rapid following Tr/J extinctions; however, species-level turnover in earliest Jurassic plant communities remained an order of magnitude higher than observed for the Triassic. We hypothesize, on the basis of evidence for geographically extensive macrofossil and palynological turnover across the entire Jameson Land Basin, that the nature and magnitude of paleoecological changes recorded in this study reflect wider vegetation change across the whole region. How exactly these changes in dominance patterns of plant primary production affected the entire ecosystem remains an important avenue of future research.

Mid-Cretaceous pCO2 based on stomata of the extinct conifer Pseudofrenelopsis (Cheirolepidiaceae)

Stomatal characteristics of an extinct Cretaceous conifer, Pseudofrenelopsis parceramosa (Fontaine) Watson, are used to reconstruct atmospheric carbon dioxide ( p CO 2 ) over a time previously inferred to exhibit major fluctuations in this greenhouse gas. Samples are from nonmarine to marine strata of the Wealden and Lower Greensand Groups of England and the Potomac Group of the eastern United States, of Hauterivian to Albian age (136–100 Ma). Atmospheric p CO 2 is estimated from the ratios between stomatal indices of fossil cuticles and those from four modern analogs (nearest living equivalent plants). Using this approach, and two calibration methods to explore ranges, results show relatively low and only slightly varying p CO 2 over the Hauterivian–Albian interval: a low of ∼560–960 ppm in the early Barremian and a high of ∼620–1200 ppm in the Albian. Data from the Barremian Wealden Group yield p CO 2 values indistinguishable from a soil-carbonate–based estimate from the same beds. The new p CO 2 estimates are compatible with sedimentological and oxygen-isotope evidence for relatively cool mid-Cretaceous climates.

Stomatal control as a driver of plant evolution

Stomata are the pores on a leaf surface through which plants regulate the uptake of carbon dioxide (CO2) for photosynthesis against the loss of water via transpiration. Turgor changes in the guard cells determine the area of stomatal pore through which gaseous diffusion can occur, thus maintaining a constant internal environment within the leaf (Gregory et al., 1950). Stomata first occurred in the fossil record ;400 million years ago (Ma), and are largely identical in form to the stomatal complexes of many extant plants, illustrating their effectiveness and importance to terrestrial plants (Edwards et al., 1998). Stomatal control is critical to a plant’s adaptation to its environment; it is this fundamental importance that has led to a wealth of stomatal research ranging in scale from biomolecular analysis to landscape processes (e.g. Gedney et al., 2006; Hu et al., 2010). The first issue of Journal of Experimental Botany, published 60 years ago, contained four papers relating to stomatal function. These included an analysis by Heath of the effects of atmospheric CO2 concentration ([CO2]) on stomatal aperture and conductance; an area of research that is increasingly relevant to our understanding of the past and prediction of future vegetation responses to atmospheric composition. Heath (1950) was the first to observe that reductions in [CO2] below ambient levels induced stomatal opening, an ecophysiological response of great interest, and that the site of CO2 sensing was most probably in the substomatal cavity and not the guard cells. Stomatal research has become vastly important to crop production, biodiversity responses, and hydrology (particularly in terms of ‘run-off’) with respect to rising atmospheric [CO2], changing water regimes, and growing populations. As our understanding of stomatal physiology develops, the role of stomata in the evolution of terrestrial vegetation and development of the terrestrial landscape and atmospheric composition is becoming increasingly evident, alongside the use of fossil stomata as palaeo-proxies of past atmospheres (e.g. McElwain et al., 2004; Berry et al., 2010; Smith et al., 2010). The stomatal control responses of plants consist of ‘shortterm’ stomatal aperture changes in response to availability of water, light, temperature, wind speed, and carbon dioxide, and also ‘longer term’ changes in stomatal density that set the limits for maximum stomatal conductance in response to atmospheric [CO2], light intensity/quality, and root-to-shoot signals of water availability (Schoch et al., 1980, 1984; Davies et al., 2000; Casson et al., 2009). Stomatal control determines the water use efficiency (WUE) of a plant by optimizing water lost against carbon gained. Additionally, the stomatal control mechanisms employed by a plant species will determine: the risk of xylem embolism by reducing the probability of cavitation through stomatal closure during episodes of high transpirative demand (Brodribb and Jordan, 2008; Meinzer et al., 2009); leaf temperature and resistance to heat stress (Srivastava et al., 1995; Jones et al., 2002); tolerance of toxic atmospheric gases (Mansfield and Majernik, 1970); nutrient uptake via promotion of root mass flow (Van Vuuren et al., 1997); and the maximum rate of photosynthesis (Korner et al., 1979). Those plant species with more effective stomatal control will be expected to be more successful than those with less effective stomatal control. However, not all plant species, or individuals within a species, possess equally effective stomatal control, in the setting of either stomatal numbers or the regulation of stomatal aperture (i.e. speed and ‘tightness’ of closure). Given that any trait that confers a selective advantage is likely to become universal within a population (McNeilly, 1968), it may be reasonable to assume that stomatal control incurs certain ‘costs’, and that these costs have played a significant role in plant evolution over the last 400 million years. The origination of major plant groups, and morphological advances such as the development of planate leaves, coincide with periods of ‘low’ atmospheric [CO2] (Fig. 1) (Woodward, 1998; Beerling et al., 2001). The reduced availability of the substrate for photosynthesis is predicted to be compensated by increases in the carboxylation efficiency of RubisCO and enhanced stomatal conductance to maintain CO2 uptake during periods of low [CO2] (Woodward, 1998; Franks and Beerling, 2009). This elevated stomatal conductance incurs higher rates of water loss and associated risks of desiccation and xylem embolism, in addition to the metabolic costs of enhanced construction of stomatal complexes. It is these costs during periods of low [CO2] that may serve as evolutionary tipping points, where species with more efficient and effective stomata and hydraulic systems are favoured (Robinson, 1994; Brodribb

Differences in the response sensitivity of stomatal index to atmospheric CO2 among four genera of Cupressaceae conifers

BACKGROUND AND AIMS The inverse relationship between stomatal density (SD: number of stomata per mm(2) leaf area) and atmospheric concentration of CO2 ([CO2]) permits the use of plants as proxies of palaeo-atmospheric CO2. Many stomatal reconstructions of palaeo-[CO2] are based upon multiple fossil species. However, it is unclear how plants respond to [CO2] across genus, family or ecotype in terms of SD or stomatal index (SI: ratio of stomata to epidermal cells). This study analysed the stomatal numbers of conifers from the ancient family Cupressaceae, in order to examine the nature of the SI-[CO2] relationship, and potential implications for stomatal reconstructions of palaeo-[CO2]. Methods Stomatal frequency measurements were taken from historical herbarium specimens of Athrotaxis cupressoides, Tetraclinis articulata and four Callitris species, and live A. cupressoides grown under CO2-enrichment (370, 470, 570 and 670 p.p.m. CO2). KEY RESULTS T. articulata, C. columnaris and C. rhomboidea displayed significant reductions in SI with rising [CO2]; by contrast, A. cupressoides, C. preissii and C. oblonga show no response in SI. However, A. cupressoides does reduce SI to increases in [CO2] above current ambient (approx. 380 p.p.m. CO2). This dataset suggests that a shared consistent SI-[CO2] relationship is not apparent across the genus Callitris. Conclusions The present findings suggest that it is not possible to generalize how conifer species respond to fluctuations in [CO2] based upon taxonomic relatedness or habitat. This apparent lack of a consistent response, in conjunction with high variability in SI, indicates that reconstructions of absolute palaeo-[CO2] based at the genus level, or upon multiple species for discrete intervals of time are not as reliable as those based on a single or multiple temporally overlapping species.

Photosynthetic diffusional constraints affect yield in drought stressed rice cultivars during flowering.

Global production of rice (Oryza sativa) grain is limited by water availability and the low ‘leaf-level’ photosynthetic capacity of many cultivars. Oryza sativa is extremely susceptible to water-deficits; therefore, predicted increases in the frequency and duration of drought events, combined with future rises in global temperatures and food demand, necessitate the development of more productive and drought tolerant cultivars. We investigated the underlying physiological, isotopic and morphological responses to water-deficit in seven common varieties of O. sativa, subjected to prolonged drought of varying intensities, for phenotyping purposes in open field conditions. Significant variation was observed in leaf-level photosynthesis rates (A) under both water treatments. Yield and A were influenced by the conductance of the mesophyll layer to CO2 (g m) and not by stomatal conductance (g s). Mesophyll conductance declined during drought to differing extents among the cultivars; those varieties that maintained g m during water-deficit sustained A and yield to a greater extent. However, the variety with the highest g m and yield under well-watered conditions (IR55419-04) was distinct from the most effective cultivar under drought (Vandana). Mesophyll conductance most effectively characterises the photosynthetic capacity and yield of O. sativa cultivars under both well-watered and water-deficit conditions; however, the desired attributes of high g m during optimal growth conditions and the capacity for g m to remain constant during water-deficit may be mutually exclusive. Nonetheless, future genetic and physiological studies aimed at enhancing O. sativa yield and drought stress tolerance should investigate the biochemistry and morphology of the interface between the sub-stomatal pore and mesophyll layer.

Coordination of stomatal physiological behavior and morphology with carbon dioxide determines stomatal control

PREMISE OF THE STUDY Stomatal control is determined by the ability to alter stomatal aperture and/or the number of stomata on the surface of new leaves in response to growth conditions. The development of stomatal control mechanisms to the concentration of CO₂within the atmosphere ([CO₂]) is fundamental to our understanding of plant evolutionary history and the prediction of gas exchange responses to future [CO₂]. METHODS In a controlled environment, fern and angiosperm species were grown in atmospheres of ambient (400 ppm) and elevated (2000 ppm) [CO₂]. Physiological stomatal behavior was compared with the stomatal morphological response to [CO₂]. KEY RESULTS An increase in [CO₂] or darkness induced physiological stomatal responses ranging from reductions (active) to no change (passive) in stomatal conductance. Those species with passive stomatal behavior exhibited pronounced reductions of stomatal density in new foliage when grown in elevated [CO₂], whereas species with active stomata showed little morphological response to [CO₂]. Analysis of the physiological and morphological stomatal responses of a wider range of species suggests that patterns of stomatal control to [CO₂] do not follow a phylogenetic pattern associated with plant evolution. CONCLUSIONS Selective pressures may have driven the development of divergent stomatal control strategies to increased [CO₂]. Those species that are able to actively regulate guard cell turgor are more likely to respond to [CO₂] through a change in stomatal aperture than stomatal number. We propose a model of stomatal control strategies in response to [CO₂] characterized by a trade-off between short-term physiological behavior and longer-term morphological response.

Increased Atmospheric SO2 Detected from Changes in Leaf Physiognomy across the Triassic–Jurassic Boundary Interval of East Greenland

The Triassic–Jurassic boundary (Tr–J; ∼201 Ma) is marked by a doubling in the concentration of atmospheric CO2, rising temperatures, and ecosystem instability. This appears to have been driven by a major perturbation in the global carbon cycle due to massive volcanism in the Central Atlantic Magmatic Province. It is hypothesized that this volcanism also likely delivered sulphur dioxide (SO2) to the atmosphere. The role that SO2 may have played in leading to ecosystem instability at the time has not received much attention. To date, little direct evidence has been presented from the fossil record capable of implicating SO2 as a cause of plant extinctions at this time. In order to address this, we performed a physiognomic leaf analysis on well-preserved fossil leaves, including Ginkgoales, bennettites, and conifers from nine plant beds that span the Tr–J boundary at Astartekløft, East Greenland. The physiognomic responses of fossil taxa were compared to the leaf size and shape variations observed in nearest living equivalent taxa exposed to simulated palaeoatmospheric treatments in controlled environment chambers. The modern taxa showed a statistically significant increase in leaf roundness when fumigated with SO2. A similar increase in leaf roundness was also observed in the Tr–J fossil taxa immediately prior to a sudden decrease in their relative abundances at Astartekløft. This research reveals that increases in atmospheric SO2 can likely be traced in the fossil record by analyzing physiognomic changes in fossil leaves. A pattern of relative abundance decline following increased leaf roundness for all six fossil taxa investigated supports the hypothesis that SO2 had a significant role in Tr–J plant extinctions. This finding highlights that the role of SO2 in plant biodiversity declines across other major geological boundaries coinciding with global scale volcanism should be further explored using leaf physiognomy.

Adaptation to high temperature mitigates the impact of water deficit during combined heat and drought stress in C3 sunflower and C4 maize varieties with contrasting drought tolerance

Heat and drought stress frequently occur together, however, their impact on plant growth and photosynthesis (PN ) is unclear. The frequency, duration and severity of heat and drought stress events are predicted to increase in the future, having severe implications for agricultural productivity and food security. To assess the impact on plant gas exchange, physiology and morphology we grew drought tolerant and sensitive varieties of C3 sunflower (Helianthus annuus) and C4 maize (Zea mays) under conditions of elevated temperature for 4 weeks prior to the imposition of water deficit. The negative impact of temperature on PN was most apparent in sunflower. The drought tolerant sunflower retained ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) activity under heat stress to a greater extent than its drought sensitive counterpart. Maize exhibited no varietal difference in response to increased temperature. In contrast to previous studies, where a sudden rise in temperature induced an increase in stomatal conductance (Gs ), we observed no change or a reduction in Gs with elevated temperature, which alongside lower leaf area mitigated the impact of drought at the higher temperature. The drought tolerant sunflower and maize varieties exhibited greater investment in root-systems, allowing greater uptake of the available soil water. Elevated temperatures associated with heat-waves will have profound negative impacts on crop growth in both sunflower and maize, but the deleterious effect on PN was less apparent in the drought tolerant sunflower and both maize varieties. As C4 plants generally exhibit water use efficiency (WUE) and resistance to heat stress, selection on the basis of tolerance to heat and drought stress would be more beneficial to the yields of C3 crops cultivated in drought prone semi-arid regions.

On the Use of Leaf Spectral Indices to Assess Water Status and Photosynthetic Limitations in Olea europaea L. during Water-Stress and Recovery

Diffusional limitations to photosynthesis, relative water content (RWC), pigment concentrations and their association with reflectance indices were studied in olive (Olea europaea) saplings subjected to water-stress and re-watering. RWC decreased sharply as drought progressed. Following rewatering, RWC gradually increased to pre-stress values. Photosynthesis (A), stomatal conductance (g s), mesophyll conductance (g m), total conductance (g t), photochemical reflectance index (PRI), water index (WI) and relative depth index (RDI) closely followed RWC. In contrast, carotenoid concentration, the carotenoid to chlorophyll ratio, water content reflectance index (WCRI) and structural independent pigment index (SIPI) showed an opposite trend to that of RWC. Photosynthesis scaled linearly with leaf conductance to CO2; however, A measured under non-photorespiratory conditions (A 1%O2) was approximately two times greater than A measured at 21% [O2], indicating that photorespiration likely increased in response to drought. A 1%O2 also significantly correlated with leaf conductance parameters. These relationships were apparent in saturation type curves, indicating that under non-photorespiratory conditions, CO2 conductance was not the major limitations to A. PRI was significant correlated with RWC. PRI was also very sensitive to pigment concentrations and photosynthesis, and significantly tracked all CO2 conductance parameters. WI, RDI and WCRI were all significantly correlated with RWC, and most notably to leaf transpiration. Overall, PRI correlated more closely with carotenoid concentration than SIPI; whereas WI tracked leaf transpiration more effectively than RDI and WCRI. This study clearly demonstrates that PRI and WI can be used for the fast detection of physiological traits of olive trees subjected to water-stress.

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.