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Cycads show no stomatal-density and index response to elevated carbon dioxide and subambient oxygen
Abstract
The stomatal density (SD) and index (SI) of fossil plants are widely used in reconstructing palaeo-atmospheric CO2 concentration (palaeo-[CO2]). These stomatal reconstructions depend on the inverse relationship between atmospheric CO2 concentration ([CO2]) and SD and/or SI. Atmospheric oxygen concentration ([O2]) has also varied throughout earth history, influencing photosynthesis via the atmospheric CO2 : O2 ratio, and possibly affecting both SD and SI. Cycads formed a major component of Mesozoic floras, and may serve as suitable proxies of palaeo-[CO2]. However, little is known regarding SD and SI responses of modern cycads to [CO2] and [O2]. SD, SI and pore length were measured in six cycad species (Cycas revoluta, Dioon merolae, Lepidozamia hopei, Lepidozamia peroffskyana, Macrozamia miquelii and Zamia integrifolia) grown under elevated [CO2] (1500 ppm) and subambient [O2] (13.0%) in combination and separately, and compared with SD, SI and pore length under control atmospheric conditions of 380 ppm [CO2] and 20.9% [O2]. The cycad species analysed showed no significant SD, SI or pore-length response to changes in [CO2] or [O2].
... Species specific SD and SI responses (in both occurrence and extent) to the availability of CO 2 can be assessed by analysis of the number of stomata and epidermal cells in the leaves of historical herbarium specimens collected during the last ~ 250 years as [CO 2 ] has risen from 280 to above 400 μmol mol −1 , [CO 2 ] enrichment studies, and over altitudinal gradients where the partial pressure of CO 2 (pCO 2 ) varies (but the concentration of CO 2 remains constant, uncoupling the effect of [CO 2 ] from CO 2 -availability) (Woodward 1987;Woodward and Bazzaz 1988;Beerling and Chaloner 1993b;Kürschner et al. 1997Kürschner et al. , 2008Kouwenberg et al. 2003;Haworth et al. 2010;Lammertsma et al. 2011;Hu et al. 2019). However, the SD and SI response to [CO 2 ] varies between species in the occurrence of any relationship (some plant groups such as the cycads do not alter SD or SI to [CO 2 ] and are known as 'SD non-responders': Haworth et al. 2011c), the extent of the SD or SI response and the [CO 2 ] range over which SD or SI responds (Beerling and Chaloner 1993a;Kürschner et al. 1996;Kürschner 1997;Haworth et al. 2013;Hu et al. 2015;Hill et al. 2019). For example, many angiosperms alter SD and SI to [CO 2 ] below 400 μmol mol −1 , but reach a 'ceiling of response' at [CO 2 ] levels above current ambient (Kürschner et al. 1996;Kürschner 1997). ...
... However, in light of the observation that A % is strongly related to stomatal responsiveness (Fig. 6c), it may be possible to infer the likelihood of a fossil plant being a SD responder on the basis of A % . If cycads are excluded (as a group cycads exhibit low A % and do not alter SD: Haworth et al. 2011c), it is possible to observe that species with an A % around 1.0-1.5% are more likely than species with an A % above 2.0% to alter stomatal initiation in response to an increase in [CO 2 ] (Fig. 8). The lack of a SD response in the cycads may be associated with their origination during a period of comparatively high-[CO 2 ] combined with an already low SD that reduces the potential of further SD adjustment and enable a minimum rate of leaf gas exchange (Haworth et al. 2011c). ...
... If cycads are excluded (as a group cycads exhibit low A % and do not alter SD: Haworth et al. 2011c), it is possible to observe that species with an A % around 1.0-1.5% are more likely than species with an A % above 2.0% to alter stomatal initiation in response to an increase in [CO 2 ] (Fig. 8). The lack of a SD response in the cycads may be associated with their origination during a period of comparatively high-[CO 2 ] combined with an already low SD that reduces the potential of further SD adjustment and enable a minimum rate of leaf gas exchange (Haworth et al. 2011c). The apparent relationship between A % and the relative change in SI is more robust than that of SD. ...
Stomata are central players in the hydrological and carbon cycles, regulating the uptake of carbon dioxide (CO 2 ) for photosynthesis and transpirative loss of water (H 2 O) between plants and the atmosphere. The necessity to balance water-loss and CO 2 -uptake has played a key role in the evolution of plants, and is increasingly important in a hotter and drier world. The conductance of CO 2 and water vapour across the leaf surface is determined by epidermal and stomatal morphology (the number, size, and spacing of stomatal pores) and stomatal physiology (the regulation of stomatal pore aperture in response to environmental conditions). The proportion of the epidermis allocated to stomata and the evolution of amphistomaty are linked to the physiological function of stomata. Moreover, the relationship between stomatal density and [CO 2 ] is mediated by physiological stomatal behaviour; species with less responsive stomata to light and [CO 2 ] are most likely to adjust stomatal initiation. These differences in the sensitivity of the stomatal density—[CO 2 ] relationship between species influence the efficacy of the ‘stomatal method’ that is widely used to infer the palaeo-atmospheric [CO 2 ] in which fossil leaves developed. Many studies have investigated stomatal physiology or morphology in isolation, which may result in the loss of the ‘overall picture’ as these traits operate in a coordinated manner to produce distinct mechanisms for stomatal control. Consideration of the interaction between stomatal morphology and physiology is critical to our understanding of plant evolutionary history, plant responses to on-going climate change and the production of more efficient and climate-resilient food and bio-fuel crops.
... The relationship between stomatal density and/or stomatal index (a ratio of the number of stomata to epidermal cells) and the atmospheric [CO 2 ] in which a leaf developed also differs between plant species, in direction, strength and the range of [CO 2 ] over which stomatal initiation is modified (Woodward 1987;Kürschner et al. 1997;Royer et al. 2001;Kouwenberg et al. 2003;Haworth et al. 2011c;Hirano et al. 2012). Many angiosperm species exhibit a ''ceiling of response'' at 350-400 ppm [CO 2 ], above which stomatal density and index no longer respond (Woodward 1987;Kürschner et al. 1997, Bettarini et al. 1998, whereas many conifers with ancient evolutionary origins often continue to reduce stomatal initiation at [CO 2 ] levels above current ambient (Kouwenberg et al. 2003;Haworth et al. 2010Haworth et al. , 2011aGrein et al. 2011). ...
... Many angiosperm species exhibit a ''ceiling of response'' at 350-400 ppm [CO 2 ], above which stomatal density and index no longer respond (Woodward 1987;Kürschner et al. 1997, Bettarini et al. 1998, whereas many conifers with ancient evolutionary origins often continue to reduce stomatal initiation at [CO 2 ] levels above current ambient (Kouwenberg et al. 2003;Haworth et al. 2010Haworth et al. , 2011aGrein et al. 2011). A similar stomatal density and stomatal index response to [CO 2 ] above 400 ppm is observed in Ginkgo biloba (Beerling et al. 1998a;Royer et al. 2001); however, atmospheric [CO 2 ] does not influence stomatal initiation in Cycadaceae (Haworth et al. 2011c). The lower ceiling of response observed in angiosperms (Woodward 1987;Kürschner et al. 1997) relative to conifers (Kouwenberg et al. 2003;Grein et al. 2011) may be associated with greater stomatal aperture control of angiosperms at [CO 2 ] above 400 ppm (Brodribb et al. 2009), possibly indicating a degree of co-ordination between physiological and morphological control of stomatal conductance in response to [CO 2 ] (Haworth et al. 2011b). ...
... Active stomatal control to C a requires investment in mechanisms for sensing of [CO 2 ], co-ordination of signals and resulting stomatal movements (Heath 1950;Hetherington and Woodward 2003;Hu et al. 2010). Plant species with highly sensitive stomata to short-term stimuli, such as members of the Cycadaceae (Fig. 3a), may not alter stomatal initiation, and thus modify stomatal density and/or stomatal index, to changes in their atmospheric environment (Marler and Willis 1997;Haworth et al. 2011c). Therefore, uptake of CO 2 is not limited by stomatal number or size during periods when conditions are favourable to photosynthesis, or constrained in their ability to respond to any future shifts in atmospheric composition via prior modification of stomatal density. ...
... Some leaf functional traits of cycads generally align with the global leaf economic spectrum, though in contrast to other vascular plants, leaf hydraulic conductance has been shown to be unrelated to the photosynthetic rate in cycads (Zhang et al., 2015). Additionally, in contrast to other major groups of vascular plants, the stomatal density of some cycad leaves does not change with elevated atmospheric CO 2 , with the exception of the stomatal number in Zamia furfuraceae, which increased with higher atmospheric CO 2 , further suggesting that cycad leaves are diverse and may have species-dependent physiological responses to changing climate (Haworth et al., 2011, Steinthorsdottir et al., 2021. These differences between cycads and other extant vascular plants suggest that xylem structure-function relationships in cycads may also differ from those observed in other vascular plants. ...
... Despite this rapid diversification during the Neogene, extinct and extant cycads are morphologically very similar, and some anatomical traits in cycads do not respond plastically to differences in atmospheric CO 2 , suggesting that the trait relationships reported here may reflect the traits of extinct cycads from long-extinct ecosystems (Haworth et al., 2011;Zhang et al., 2015). The fossils of extant Cycadales, however, are limited to the Cenozoic (Coiro & Pott, 2017) when angiosperms started to prosper (Condamine et al., 2015;Simonin & Roddy, 2018). ...
Interconduit pit membranes, which are permeable regions in the primary cell wall that connect to adjacent conduits, play a crucial role in water relations and the movement of nutrients between xylem conduits. However, how pit membrane characteristics might influence water-carbon coupling remains poorly investigated in cycads. We examined pit characteristics, the anatomical and photosynthetic traits of thirteen cycads from a common garden, to determine if pit traits and their coordination are related to water relations and carbon economy. We found that the pit traits of cycads were highly variable and that cycads exhibited a similar tradeoff between pit density and pit area as other plant lineages. Unlike other plant lineages (1) pit membranes, pit apertures, and pit shapes of cycads were not coordinated as in angiosperms; (2) cycads exhibited larger pit membrane areas but lower pit densities relative to ferns and angiosperms, but smaller and similar pit membrane densities to non-cycad gymnosperms; (3) cycad pit membrane areas and densities were partially coordinated with anatomical traits, with hydraulic supply of the rachis positively coordinated with photosynthesis, while pit aperture areas and fractions were negatively coordinated with photosynthetic traits; (4) cycad pit traits reflected adaptation to wetter habitats for Cycadaceae and drier habitats for Zamiaceae. The large variation in pit traits, the unique pit membrane size and density, and the partial coordination of pit traits with anatomical and physiological traits of the rachis and pinna among cycads may have facilitated their dominance in a variety of ecosystems from the Mesozoic to modern times. This article is protected by copyright. All rights reserved.
... A physiological connection between the guard cells and subsidiary cells is well known in grasses, where the lateral subsidiary cells are involved in the mechanisms of stomatal opening via exchange of osmolytes with the guard cells (Franks and Farquhar, 2007;Raissig et al., 2017;Gray et al., 2020). Some authors have reported a relatively rapid mechanism of closure and opening and high water efficiency in the Cycadales (Haworth et al., 2011;Álvarez-Yépiz et al., 2017). On the other hand, encircling cells and polar cells are almost completely sclerified at maturity in all genera except Stangeria, in which they contain oxalate crystals. ...
... The similarity between early development of the epidermis in cycads and other gymnosperms suggests that the lack of response of cycad stomatal density to CO 2 (Haworth et al., 2011) might not be linked to developmental constraints. Further physiological studies are needed, including electrophysiological investigations, stomatal mechanics, and response to desiccation or abscisic acid, to test whether the responses of cycad stomata differ radically from those of the more efficient angiosperm stomata. ...
Background and Aims
The gymnosperm order Cycadales is pivotal for our understanding of seed-plant phylogeny because of its phylogenetic placement close to the root node of extant spermatophytes and its combination of both derived and plesiomorphic character states. Although widely considered a ‘living fossil’ group, extant cycads display a high degree of morphological and anatomical variation. We investigate stomatal development in Zamiaceae to evaluate variation within the order and homologies between cycads and other seed plants.
Methods
Leaflets of seven species across five genera representing all major clades of Zamiaceae were examined at various stages of development using light microscopy and confocal microscopy.
Key Results
All genera examined have lateral subsidiary cells of perigenous origin that differ from other pavement cells in mature leaflets and could have a role in stomatal physiology. Early epidermal patterning in a “quartet” arrangement occurs in Ceratozamia, Zamia, and Stangeria. Distal encircling cells, which are sclerified at maturity, are present in all genera except Bowenia, which has relatively rapid elongation and differentiation of the pavement cells during leaflet development.
Conclusions
Stomatal structure and development in Zamiaceae highlights some traits that are plesiomorphic in seed plants, including the presence of perigenous encircling subsidiary cells, and shows a clear difference between the developmental trajectories of cycads and Bennettitales. Our study also shows an unexpected degree of variation among subclades in the family, potentially linked to differences in leaflet development and suggesting convergent evolution in cycads.
... Stomatal density has previously been shown to be negatively correlated with pCO 2 (Woodward, 1987;Woodward and Kelly, 1995;Royer, 2001;Barclay and Wing, 2016) and based on optimization theory we may expect a similar relationship between SD and sub-ambient O 2 as we would for elevated CO 2 . However, studies in relation to SD or SI response to O 2 have revealed contradictory results with some showing a positive (Beerling et al., 1998a(Beerling et al., , 1998bHaworth et al., 2013), no change (Haworth et al., 2011(Haworth et al., , 2013 or negative correlation (Ramonell et al., 2001). In this study, four out of nine species showed a trend towards decreased stomatal density in the high CO 2 treatment, although, P. salignus was the only species to demonstrate a statistically significant change. ...
... Similarly, in low O 2 , four of the nine species showed a decrease in SD but only O. regalis displayed a decrease (the largest) that was statistically significant (Fig. 3). This SD response to low O 2 (non or positive correlation) is in agreement with previous studies (Beerling et al., 1998a(Beerling et al., , 1998bHaworth et al., 2011Haworth et al., , 2013 but contradicts that of Ramonell et al. (2001). It is worth noting however, that the study carried out by Ramonell et al. (2001) demonstrated that a small decline in O 2 can have varying responses between replicas of A. thaliana. ...
A drive to improve long-term estimates of atmospheric CO2 change through Earths history has led to the development of novel paleoproxy CO2 methods applicable to fossil plants. This paper compares two of these paleoproxy CO2 methods (1) the empirical model of Schubert and Jahren (2012, 2015) termed the C3 plant proxy, which was developed using the hyperbolic relationship observed between plant carbon isotope discrimination (Δ¹³C) and pCO2 and (2) the mechanistic model of Franks et al. (2014), which utilizes stomatal anatomy measurements and plant carbon isotopic composition and is based on established equations for leaf gas exchange and photosynthesis. To date both models lack detailed experimental testing of the robustness and accuracy of their pCO2 predictions in relation to phylogenetic differences in Δ¹³C between C3 plant groups and/or species and atmospheric O2 concentration, which has co-fluctuated with CO2 in the geological past. Here, we investigate if these novel paleoproxy CO2 approaches can produce phylogenetically independent estimates of pCO2 that are not influenced by variations in atmospheric oxygen. To address this, model estimates of pCO2 were compared with measured CO2 values for ten plant species representing four major vascular plant groups (lycophytes, monilophytes, gymnosperms and angiosperms) grown for 6 months in walk-in plant growth chambers under varying O2:CO2 ratios. Results from the mechanistic model reveal that species-specific plant responses to atmospheric CO2 accounted for the large variability in CO2 predictions between species and overestimations of pCO2 by ∼+232 ppm to 940 ppm. Adjustments to the model that involved: (1) corrections to the photorespiratory compensation point (to account for fluctuating oxygen) and (2) removal of the phylogenetic effect on Δ¹³C, reduced between-species variability (by 50%) and led to better pCO2 estimates within 58–229 ppm of measured values. The C3 plant proxy (empirical approach) produced accurate CO2 estimates within +37 to +71 ppm of measured values, however it was affected by species-specific differences in Δ¹³C and for some species resulted in negative estimates of pCO2. Sub-ambient O2 (16%) resulted in erroneously high CO2 estimates (∼100 ppm higher than the control) for a number of species, as plant responses to decreasing O2 mimicked those of increasing CO2. We conclude that both models (with phylogenetic corrections to Franks et al. (2014)) can produce accurate estimates of paleo-CO2 when a mix of three to four species, preferably containing representatives from both pteridophytes and spermatophytes, is used to obtain a consensus pCO2 estimate. We advocate a fossil assemblage rather than a single-species approach to paleo-CO2 estimation in future application of either method.
... The range of stomatal density and size reported in this study ( fig. 3) is similar to that found for cycads in other studies, but it is considerably higher than in most angiosperms (e.g., Drake et al. 2013). Haworth et al. (2011) reported a range of stomatal densities for six cycad species of 30-80 stomata mm 22 , whereas the results of this study found stomatal density of Bowenia species to be 18-107 stomata mm 22 . This is a much larger range than that found by Haworth et al. (2011), and this large range is due to changes in one of the extant species, Bowenia spectabilis. ...
... Haworth et al. (2011) reported a range of stomatal densities for six cycad species of 30-80 stomata mm 22 , whereas the results of this study found stomatal density of Bowenia species to be 18-107 stomata mm 22 . This is a much larger range than that found by Haworth et al. (2011), and this large range is due to changes in one of the extant species, Bowenia spectabilis. All other Bowenia and Eobowenia incrassata had a range of between 3 and 50 stomata mm 22 . ...
Premise of research. This study compares the pinnule morphology of three fossil Bowenia species, one Eobowenia (fossil) species, and several Bowenia fossil pinnule fragments with the two extant Bowenia species. Methodology. Pinnule area, stomatal density, and size have been measured on fossil and extant specimens. Measures have been correlated with solar radiation and temperature to ascertain any correlations. Environment and climate variables have been chosen, as they have changed since the Eocene and Lower Cretaceous when the Australian and South American fossils were growing. Pivotal results. Two of the fossil Bowenia species and Eobowenia have significantly smaller pinnules than the living species, and all the fossils have relatively small and sparse stomata compared with the living species. Extant Bowenia pinnule area is positively correlated with daily radiation and temperature. Conclusions. Those fossil species with small pinnules likely lived in relatively dark environments where small pinnules aided the capture of sunflecks and/or facilitated light capture. The smaller and sparser stomata may have limited the potential sites for fungal invasion in the extremely humid growth conditions without hampering overall growth rates in the prevailing very high atmospheric CO 2 levels.
... Jordan (2011) suggested that high species variability in the magnitude and sign of stomatal density response to CO 2 between different species weakens the reliability of stomatal-based CO 2 proxies because it breaks the key assumption of evolutionary conservatism. We agree that this is the case for a number of families that have been investigated (Kelly and Beerling, 1995;Kürschner et al., 1997;Haworth et al., 2010); however, other families show strong conservatism in the SD-CO 2 relationship with species belonging to the same genera, and even at the family or order level, clustering together with similar SD/SI values, as well as displaying similar response directions and magnitudes to changes in pCO 2 (McElwain et al., 2002;Barclay et al., 2010;Haworth et al., 2011;Steinthorsdottir et al., 2011a;Steinthorsdottir et al., 2011b;Steinthorsdottir et al., 2016b). This is particularly important when operating in the pre-quaternary fossil record, which does not typically offer fossil plants that are conspecific with modern plants. ...
... Of interest from the perspective of this review is the likely physiological significance of different developmental pathways, if any. Paleo-pCO 2 proxies based on empirical relationships between SD and SI responses to pCO 2 are limited by the fact that some taxa are CO 2 sensitive in their developmental response , while others are not (Haworth et al., 2011). To date, no study has investigated if the stomatal density response to CO 2 is modulated in some way by the different developmental pathways of the stomatal complex. ...
http:/ / dx. doi. org/ 10. 1104/ pp. 17. 00204
... Indeed, it is not well-known whether cycad leaves show strong variation in physiology, or whether that variation would be constrained by similar principles as in angiosperms. In contrast to typical angiosperms, cycads have no response in stomatal density to elevated CO 2 (Haworth et al., 2011) suggesting that they may have a relatively inflexible leaf design and physiology compared with angiosperms. The aim of this study was to assess for cycads the association of traits with photosynthetic rate, as expected based on studies of angiosperms, conifers, ferns and mosses ( Fig. 1), including nutrient composition, leaf structure, stomatal conductance and leaf hydraulics. ...
... A recent molecular dating study suggested that the extant cycads are not older than c. 12 Myr (Nagalingum et al., 2011). However, we hypothesize that these trait relationships first evolved in the ancient cycads and remain in modern cycads because first, cycads show relative morphological, and potentially, physiological stability in the face of long-term climate change (Haworth et al., 2011), and second, fossil and extant cycads have strong morphological similarities. ...
Cycads are the most ancient lineage of living seed plants, but the design of their leaves has received little study. We tested whether cycad leaves are governed by the same fundamental design principles previously established for ferns, conifers and angiosperms, and characterized the uniqueness of this relict lineage in foliar trait relationships.
Leaf structure, photosynthesis, hydraulics and nutrient composition were studied in 33 cycad species from nine genera and three families growing in two botanical gardens.
Cycads varied greatly in leaf structure and physiology. Similarly to other lineages, light‐saturated photosynthetic rate per mass ( A m ) was related negatively to leaf mass per area and positively to foliar concentrations of chlorophyll, nitrogen (N), phosphorus and iron, but unlike angiosperms, leaf photosynthetic rate was not associated with leaf hydraulic conductance. Cycads had lower photosynthetic N use efficiency and higher photosynthetic performance relative to hydraulic capacity compared with other lineages.
These findings extend the relationships shown for foliar traits in angiosperms to the cycads. This functional convergence supports the modern synthetic understanding of leaf design, with common constraints operating across lineages, even as they highlight exceptional aspects of the biology of this key relict lineage.
... Some exceptions to the general rule of the inverse response of stomatal frequency to pCO 2 have been found, most notably in the cycads, which display little or no change in SI with raised pCO 2 (Haworth et al., 2011b(Haworth et al., , 2013. Experimental data showed that cycads do adapt to high pCO 2 , but respond primarily physiologically (reducing stomatal conductance by closing of stomata), rather than morphologically (reduced SI), both of which responses aim to conserve WUE (Haworth et al., 2011b). ...
... Some exceptions to the general rule of the inverse response of stomatal frequency to pCO 2 have been found, most notably in the cycads, which display little or no change in SI with raised pCO 2 (Haworth et al., 2011b(Haworth et al., , 2013. Experimental data showed that cycads do adapt to high pCO 2 , but respond primarily physiologically (reducing stomatal conductance by closing of stomata), rather than morphologically (reduced SI), both of which responses aim to conserve WUE (Haworth et al., 2011b). Only the morphological response is detectable in sub-fossil and fossil plants and therefore cycads and any other plant groups that respond primarily physiologically to pCO 2 should not be utilized in palaeo-pCO 2 reconstructions. ...
... More evidence is needed to further characterize these hydraulic strategies and how they may be linked to climate preferences. More generally, conifer species differing in their degree of isohydry vs anisohydry exhibit different stomatal behaviors mediated by abscisic acid concentrations (Brodribb et al., 2014), but work on stomatal physiology in cycads has been limited (Haworth et al., 2011). ...
Drought‐induced xylem embolism is a primary cause of plant mortality. Although c. 70% of cycads are threatened by extinction and extant cycads diversified during a period of increasing aridification, the vulnerability of cycads to embolism spread has been overlooked.
We quantified the vulnerability to drought‐induced embolism, pressure–volume curves, in situ water potentials, and a suite of xylem anatomical traits of leaf pinnae and rachises for 20 cycad species. We tested whether anatomical traits were linked to hydraulic safety in cycads.
Compared with other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than noncycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads.
Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits – particularly vessels – may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.
... Seventeen out of twenty-six species showed a decrease in SD and increase in SS (Fig. 9), possibly contributing to the similarity between the SS-SD relationship in ambient and elevated [CO 2 ] (Fig. 7b). In this case, the species that did not reduce SD and increase SS exhibited strongly active physiological stomatal behaviour in response to fluctuating light conditions and instantaneous increases in [CO 2 ] (Haworth et al., 2011c;Haworth et al., 2013;Haworth et al., 2015). Excluding these species with strongly active stomatal behaviour, it may be possible to propose that SS and SD vary in co-ordination over a tight range in response to atmospheric [CO 2 ] (Fig. 9). ...
The limits for stomatal conductance are set by stomatal size (SS) and density (SD). An inverse relationship between SS and SD has been observed in fossil and living plants. This has led to hypotheses proposing that the ratio of SS to SD influences the diffusion pathway for CO2 and degree of physiological stomatal control. However, conclusive evidence supportive of a functional role of the SS-SD relationship is not evident, and patterns in SS-SD may simply reflect geometric constraints in stomatal spacing over a leaf surface. We examine published and new data to investigate the potential functional significance of the relationship between SS and SD to atmospheric [CO2] in multiple generation adaptive responses and short-term acclamatory adjustment of stomatal morphology. Consistent patterns in SS and SD were not evident in fossil and living plants adapted to high [CO2] over many generations. However, evolutionary adaptation to [CO2] strongly affected SS and SD responses to elevated [CO2], with plants adapted to the 'low' [CO2] of the past 10 million years (Myr) showing adjustment of SS-SD, while members of the same species adapted to 'high' [CO2] showed no response. This may suggest that SS and SD responses to future [CO2] will likely constrain the stimulatory effect of 'CO2-fertilisation' on photosynthesis. Angiosperms generally possessed higher densities of smaller stomata that corresponded to a greater degree of physiological stomatal control consistent with selective pressures induced by declining [CO2] over the past 90 Myr. Atmospheric [CO2] has likely shaped stomatal size and density relationships alongside the interaction with stomatal physiological behaviour. The rate and predicted extent of future increases in [CO2] will have profound impacts on the selective pressures shaping SS and SD. Understanding the trade-offs involved in SS-SD and the interaction with [CO2], will be central to the development of more productive climate resilient crops.
... To date, the most widely used proxies to estimate palaeo-CO 2 levels have been Ginkgo biloba and Metasequoia glyptostroboides, since both species exhibit ideal inverse SF-pCO 2 correlations and have abundant fossil relatives stretching as far back as the Cretaceous Period (Retallack, 2001(Retallack, , 2009Royer et al., 2001b;Beerling and Royer, 2002a;Quan et al., 2009;Smith et al., 2010;Doria et al., 2011;Wang et al., 2015;Barclay and Wing, 2016). Other species, including other conifers (Passalia, 2009;Steinthorsdottir and Vajda, 2013;Liu et al., 2016), cycads (McElwain et al., 1999;Haworth et al., 2011b), Quercus petraea (van der Burgh et al., 1993;Kürschner et al., 1996), Q. guyavifolia (Hu et al., 2015;Huang et al., 2016), members of the Lauraceae (McElwain, 1998;Greenwood et al., 2003;Kürschner et al., 2008) and Betula species (Finsinger and Wagner-Cremer, 2009), have been used as proxies much less frequently because of their limited number of fossil relatives. Clearly, identification of additional proxies that are sensitive to atmospheric pCO 2 and also have numerous fossil relatives is highly desirable. ...
Background and aims:
The inverse correlation between atmospheric CO2 partial pressure (pCO2) and stomatal frequency in many plants has been widely used to estimate palaeo-CO2 levels. However, apparent discrepancies exist among the obtained estimates. This study attempts to find a potential proxy for palaeo-CO2 concentrations by analysing the stomatal frequency of Quercus glauca (section Cyclobalanopsis, Fagaceae), a dominant species in East Asian sub-tropical forests with abundant fossil relatives.
Methods:
Stomatal frequencies of Q. glauca from three material sources were analysed: seedlings grown in four climatic chambers with elevated CO2 ranging from 400 to 1300 ppm; extant samples collected from 14 field sites at altitudes ranging from 142 to 1555 m; and 18 herbarium specimens collected between 1930 and 2011. Stomatal frequency-pCO2 correlations were determined using samples from these three sources.
Key results:
An inverse correlation between stomatal frequency and pCO2 was found for Q. glauca through cross-validation of the three material sources. The combined calibration curves integrating data of extant altitudinal samples and historical herbarium specimens improved the reliability and accuracy of the curves. However, materials in the climatic chambers exhibited a weak response and relatively high stomatal frequency possibly due to insufficient treatment time.
Conclusions:
A new inverse stomatal frequency-pCO2 correlation for Q. glauca was determined using samples from three sources. These three material types show the same response, indicating that Q. glauca is sensitive to atmospheric pCO2 and is an ideal proxy for palaeo-CO2 levels. Quercus glauca is a nearest living relative (NLR) of section Cyclobalanopsis fossils, which are widely distributed in the strata of East Asia ranging from the Eocene to Pliocene, thereby providing excellent materials to reconstruct the atmospheric CO2 concentration history of the Cenozoic. Quercus glauca will add to the variety of proxies that can be widely used in addition to Ginkgo and Metasequoia.
... Recent studies indicate that different plants show different responses corresponding to the change in atmospheric CO 2 concentrations (Royer et al. 2001;Haworth et al. 2010Haworth et al. , 2011Field et al. 2015). By analyzing the stomatal values for conifers from the ancient family cupressaceae (Athrotaxis cupressoides, Tetraclinis articulate, and four Callitris species, i.e., C. oblonga, C. preissii, C. rhomboidea, and C. columnaris), a relation between stomatal index (SI) and CO 2 can be defined. ...
The extinct conifer family Cheirolepidiaceae, especially Pseudofrenelopsis, is commonly used to reconstruct the atmospheric palaeo-CO2 concentration (pCO2) during the Cretaceous period. In recent years, many Pseudofrenelopsis specimens have been collected from the uppermost stratum of the Naijiahe Formation in the Liupanshan Basin, Ningxia Hui Autonomous Region, Northwest China. The stomatal parameters, such as stomatal density, stomatal index, stomatal pore length, and stomatal pore depth, and the stable carbon isotope composition of the present Pseudofrenelopsis were analyzed. The palaeo-CO2 levels of the Liupanshan Basin during the late Early Cretaceous (late Albian) were reconstructed using stomatal ratio (SR) and mechanistic model approaches. The SR method yielded a semi-quantitative pCO2 estimate of 620 ppmv on the basis of the Recent standardization and 1030 ppmv on the basis of the Carboniferous standardization, which show similarities with other SR-based and geochemical-based reconstructions for the late Early Cretaceous. The pCO2 was about 670 ppmv on the basis of mechanistic model method, similar to the estimated pCO2 values recovered by the SR method corrected with the Recent standardization. Based on comparative studies of previously published pCO2 results of the Early Cretaceous, pCO2 levels varied during the Early Cretaceous, and pCO2 was relatively stable during the late Early Cretaceous. Furthermore, environmental conditions of the Liupanshan Basin during the late Early Cretaceous were studied. The stable carbon isotope composition of Pseudofrenelopsis leaves ranged from −21.5‰ to −24.3‰, with an average of −22.8‰, indicating an arid/semi-arid and high-evaporation climate during the late Early Cretaceous in the Liupanshan Basin. These environmental conditions were also supported by palynological, lithological, and geochemical evidence.
... This phenomenon has been observed by a literature survey of 65 SI responses (from a pool of 35 species) to experimental CO 2 enrichment (usually 2 × ambient) in which it is reported that 66% of cases showed no significant response, with 29% showing a reduction and 5% showing an increase (Royer, 2001;Royer et al., 2001). Besides, six cycad species analyzed by Haworth et al. (2011) also showed no significant SI response to changes in CO 2 concentration. Additionally, SI is related to SD, which actually changes over longer time periods, from phenotypic changes expressed during the lifespan of individuals to evolutionary changes within lineages (Wagner et al., 1996;Gray et al., 2000;Royer, 2001). ...
... This phenomenon has been observed by a literature survey of 65 SI responses (from a pool of 35 species) to experimental CO 2 enrichment (usually 2 × ambient) in which it is reported that 66% of cases showed no significant response, with 29% showing a reduction and 5% showing an increase (Royer, 2001;Royer et al., 2001). Besides, six cycad species analyzed by Haworth et al. (2011) also showed no significant SI response to changes in CO 2 concentration. Additionally, SI is related to SD, which actually changes over longer time periods, from phenotypic changes expressed during the lifespan of individuals to evolutionary changes within lineages (Wagner et al., 1996;Gray et al., 2000;Royer, 2001). ...
Recently, several leaf fossils with good cuticles were discovered from the Oligocene deposits in Guangxi, China. The high fossilization potential of these leaves and easily identifiable stomata and epidermal cells make them an excellent source for CO2 reconstruction. In this study, atmospheric CO2 of the Oligocene is reconstructed using the mechanistic-theoretical model based on stomatal data, photosynthesis and gas exchange control and using an alternative method based only on stomatal ratio. Fossil leaves of Buxus ningmingensis, Chuniophoenix slenderifolius and Cephalotaxus ningmingensis, two angiosperms and one gymnosperm, were considered. It was found that some differences were present between the results obtained by the two methods. The SR-based method yields a somewhat narrower CO2 range (from 355 to 578 ppmv) than the model approach (from 255 to 972 ppmv) which encloses the former range. The CO2 results derived from the three species using the two approaches are overlapped to a high degree with CO2 data from other terrestrial plants and phytoplankton material. More data provided by different proxies are desirable to unravel the interactions between atmospheric CO2 and climate change for the Oligocene.
... This hypothesis was tested on angiosperm and coniferous gymnosperm species; however, ferns and cycads were excluded (Robinson, 1994). In contrast to angiosperms, cycads are an ancient plant group (Jones, 2002;Nagalingum et al., 2011) with slow reproductive biology, long leaf lifespan, and relatively large stomata (Haworth et al., 2011); the question remains whether their large stomata are less efficient than the smaller stomata of angiosperms in our currently low CO 2 world. Cowan (1977) and Cowan and Farquhar (1977) hypothesized that plants display optimal stomatal behavior, defined as maximizing photosynthetic gain to water loss. ...
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.
... Besides, the epidermal structure of Taeniopteris cf. multinervis Weiss is similar to living cycads (Haworth et al., 2011;Mickle et al., 2011) and Nilssonia Brongniart, a fossil cycadalean genus. Furthermore, the seeds with similar morphology to those attached to Crossozamia chinensis (Zhu et Du) Gao et Thomas (Fig. 3F) are associated with T. cf. ...
Taeniopteris Brongniart is widespread all over the world and is one of the most common elements in the Permian Cathaysian floras of northern China. However, its systematic position is largely unknown because of lacking anatomical information. Based on materials from the lower Permian of Baode, Shanxi, cuticle anatomy of Taeniopteris cf. multinervis Weiss is examined for the first time. Leaves are linear, entire-margined with obtuse apex, tapered base and 2-3 times bifurcated lateral veins. Haplocheilic stomata are present on both adaxial and abaxial cuticles. Adaxial cuticle is moderately thick, and stomata are arranged in rows on the midrib and lateral vein bases, and irregularly in the intercostal fields. Abaxial cuticle is extremely thin, and stomata are also distributed in rows on the midrib, and irregularly in the intercostal fields. Morphological and epidermal characteristics as well as associated seeds suggest Taeniopteris cf. multinervis Weiss probably has cycadalean affinity, although pteridosperm cannot be excluded. Taeniopteris cf. multinervis Weiss is probably a tropical rain forest understory species with a river-side habitat, and well adapted to a humid environment based on its thin abaxial cuticle, unsunken stomata and water-repellent adaxial surface.
... Given the signifi cance of stomatal control to the success of an individual plant or species, it may be assumed that the benefi ts of more effective stomatal control would confer a selective advantage to an individual and as a result become more widespread ( Haworth et al., 2011a ;Assouline and Or, 2013 ). However, a remarkable diversity of stomatal control strategies is observed across ancient basal and derived vascular plants lineages ( Franks and Farquhar, 2007 ;Brodribb et al., 2009 ;Haworth et al., 2011bHaworth et al., , 2013Ruszala et al., 2011 ;Tomimatsu and Tang, 2012 ). It may therefore be inferred that plants are subject to evolutionary selective pressures exerted by a tradeoff between the costs and benefi ts of respective stomatal control strategies ( Haworth et al., 2011a ). ...
•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 CO2 within the atmosphere ([CO2]) is fundamental to our understanding of plant evolutionary history and the prediction of gas exchange responses to future [CO2]. •
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]. •
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. •
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.
© 2015 Botanical Society of America, Inc.
... This serves to maximize water use efficiency under high [CO 2 ] and to ensure optimal photosynthesis (Brodribb and McAdam, 2013). Some groups of land plants, however, including cycads, other gymnosperms and ferns, have recently been found to be unresponsive to such changes in [CO 2 ] (Brodribb et al., 2009;Haworth et al., 2011). To date, similar studies examining stomatal responses to [CO 2 ], including those relevant to plant evolutionary timescales (e.g. ...
Following the consensus view for unitary origin and conserved function of stomata across over 400 million years of land plant evolution, stomatal abundance has been widely used to reconstruct palaeo-atmospheric environments. However, the responsiveness of stomata in mosses and hornworts, the most basal stomate lineages of extant land plants, has received relatively little attention. This study aimed to redress this imbalance and provide the first direct evidence of bryophyte stomatal responsiveness to atmospheric CO2.
A selection of hornwort (Anthoceros punctatus, Phaeoceros laevis) and moss (Polytrichum juniperinum, Mnium hornum, Funaria hygrometrica) sporophytes with contrasting stomatal morphologies were grown under different atmospheric CO2 concentrations ([CO2]) representing both modern (440 p.p.m. CO2) and ancient (1500 p.p.m. CO2) atmospheres. Upon sporophyte maturation, stomata from each bryophyte species were imaged, measured and quantified.
Densities and dimensions were unaffected by changes in [CO2], other than a slight increase in stomatal density in Funaria and abnormalities in Polytrichum stomata under elevated [CO2].
The changes to stomata in Funaria and Polytrichum are attributed to differential growth of the sporophytes rather than stomata-specific responses. The absence of responses to changes in [CO2] in bryophytes is in line with findings previously reported in other early lineages of vascular plants. These findings strengthen the hypothesis of an incremental acquisition of stomatal regulatory processes through land plant evolution and urge considerable caution in using stomatal densities as proxies for paleo-atmospheric CO2 concentrations.
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... The method has been widely used to estimate palaeo-CO 2 levels by applying the correlation to closely related plant fossils. Numerous genera and species have been used, such as Ginkgo (Retallack, 2001;Royer et al., 2001b;Beerling and Royer, 2002a;Retallack, 2009;Smith et al., 2010), Metasequoia (Royer et al., 2001b;Doria et al., 2011), other conifers (Passalia, 2009;Steinthorsdottir andVajda, 2013), cycads (McElwain et al., 1999;Haworth et al., 2011b), Quercus (van der Burgh et al., 1993Kürschner et al., 1996), Lauraceae (McElwain, 1998Greenwood et al., 2003;Kürschner et al., 2008) and Betula (Finsinger and Wagner-Cremer, 2009). The precision of identifying nearest living relatives (NLRs) of fossil species and the accuracy of the correlation between stomatal frequency and pCO 2 can have profound effects on the estimates because the relationship is species specific. ...
The inverse relationship between atmospheric CO2 partial pressure (pCO2) and stomatal frequency in many species of plants has been widely used to estimate palaeoatmospheric CO2 (palaeo-CO2) levels; however, the results obtained have been quite variable. This study attempts to find a potential new proxy for palaeo-CO2 levels by analysing stomatal frequency in Quercus guyavifolia (Q. guajavifolia, Fagaceae), an extant dominant species of sclerophyllous forests in the Himalayas with abundant fossil relatives.
Stomatal frequency was analysed for extant samples of Q. guyavifolia collected from17 field sites at altitudes ranging between 2493 and 4497 m. Herbarium specimens collected between 1926 and 2011 were also examined. Correlations of pCO2-stomatal frequency were determined using samples from both sources, and these were then applied to Q. preguyavaefolia fossils in order to estimate palaeo-CO2 concentrations for two late-Pliocene floras in south-western China.
In contrast to the negative correlations detected for most other species that have been studied, a positive correlation between pCO2 and stomatal frequency was determined in Q. guyavifolia sampled from both extant field collections and historical herbarium specimens. Palaeo-CO2 concentrations were estimated to be approx. 180-240 ppm in the late Pliocene, which is consistent with most other previous estimates.
A new positive relationship between pCO2 and stomatal frequency in Q. guyavifolia is presented, which can be applied to the fossils closely related to this species that are widely distributed in the late-Cenozoic strata in order to estimate palaeo-CO2 concentrations. The results show that it is valid to use a positive relationship to estimate palaeo-CO2 concentrations, and the study adds to the variety of stomatal density/index relationships that available for estimating pCO2. The physiological mechanisms underlying this positive response are unclear, however, and require further research.
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... Although the plant gene HIC signaling pathway, which encodes a negative regulator of stomatal development that responds to pCO 2 concentrations, has been mapped (Gray et al., 2000;Lake et al., 2002) and a large majority of (in particular gymnosperm) woody plants has been shown to react to elevated pCO 2 (Royer, 2001;Haworth et al., 2013), some plant taxa do not respond by lowering their stomatal densities with elevated pCO 2 (e.g. Haworth et al., 2011b). To obtain optimal results, we propose that only proven responders among modern analog taxa should be used in paleo-pCO 2 reconstructions. ...
The stomatal index (a measure of stomatal density) of an extinct Australian Early Jurassic araucariacean conifer species, Allocladus helgei Jansson, is used to reconstruct the atmospheric carbon dioxide concentration (pCO2) in the Early Jurassic. The fossil leaves are preserved in a single bed, palynologically dated to late Pliensbachian (~185–183 Mya). Atmospheric pCO2 is estimated from the ratios between the stomatal index of A. helgei and the stomatal indices of three modern analogs (nearest living equivalent plants). CO2 concentration in the range of ~750–975 ppm was calibrated from the fossil material, with a best-estimated mean of ~900 ppm. The new average pCO2 determined for the late Pliensbachian is thus similar to, although ~10% lower, than previously inferred minimum concentrations of ~1000, based on data from the Northern Hemisphere, but may help constrain pCO2 during this period. Our results are the first pCO2 estimates produced using Jurassic leaves from the Southern Hemisphere and showthat i) paleo-atmospheric pCO2 estimates are consistent at a global scale, though more investigations of Southern Hemisphere material are required, and ii) the stomatal proxy method can now be used without the context of relative change in pCO2 when applying the correct methodology.
... Although the plant gene HIC signaling pathway, which encodes a negative regulator of stomatal development that responds to pCO 2 concentrations, has been mapped (Gray et al., 2000;Lake et al., 2002) and a large majority of (in particular gymnosperm) woody plants has been shown to react to elevated pCO 2 (Royer, 2001;Haworth et al., 2013), some plant taxa do not respond by lowering their stomatal densities with elevated pCO 2 (e.g. Haworth et al., 2011b). To obtain optimal results, we propose that only proven responders among modern analog taxa should be used in paleo-pCO 2 reconstructions. ...
The stomatal index (a measure of stomatal density) of an extinct Australian Early Jurassic araucariacean conifer species, Allocladus helgei Jansson, is used to reconstruct the atmospheric carbon dioxide concentration (pCO2) in the Early Jurassic. The fossil leaves are preserved in a single bed, palynologically dated to late Pliensbachian (~ 185–183 Mya). Atmospheric pCO2 is estimated from the ratios between the stomatal index of A. helgei and the stomatal indices of three modern analogs (nearest living equivalent plants). CO2 concentration in the range of ~ 750–975 ppm was calibrated from the fossil material, with a best-estimated mean of ~ 900 ppm. The new average pCO2 determined for the late Pliensbachian is thus similar to, although ~ 10% lower, than previously inferred minimum concentrations of ~ 1000, based on data from the Northern Hemisphere, but may help constrain pCO2 during this period. Our results are the first pCO2 estimates produced using Jurassic leaves from the Southern Hemisphere and show that i) paleo-atmospheric pCO2 estimates are consistent at a global scale, though more investigations of Southern Hemisphere material are required, and ii) the stomatal proxy method can now be used without the context of relative change in pCO2 when applying the correct methods.
... Using the stomatal index technique, Wan et al. (2011) and Quan et al. (2009) reconstructed CO 2 levels in the Santonian through Campanian by both RF and NLE methods based on one fossil species, Ginkgo adiantoides, from a single profile. In comparison to multispecies-based CO 2 reconstructions, the monospecies-based reconstruction minimizes potential bias produced by data using different species, because the stomata-CO 2 response is species-specific (Royer, 2001;Haworth et al., 2010Haworth et al., , 2011. RF-based CO 2 estimates from the SI analyses vary from~661 ppm in the early Santonian to~531 ppm in the middle and~565 ppm in the late Santonian. ...
... However, evidence of abscisic acid and [CO 2 ] sensitivity in the stomatal aperture response of the ancient lycophyte Selaginella uncinata (Ruszala et al. 2011) and moss Physcomitrella patens (Chater et al. 2011) do not support this interpretation. The relationship between stomatal density and/or stomatal index (a ratio of the number of stomata to epidermal cells) and the atmospheric [CO 2 ] in which a leaf developed also differs between plant species, in direction, strength and the range of [CO 2 ] over which stomatal initiation is modified (Woodward 1987; Kürschner et al. 1997; Royer et al. 2001; Kouwenberg et al. 2003; Haworth et al. 2011c; Hirano et al. 2012). Many angiosperm species exhibit a ''ceiling of response'' at 350–400 ppm [CO 2 ], above which stomatal density and index no longer respond (Woodward 1987; Kürschner et al. 1997, 2008, Bettarini et al. 1998), whereas many conifers with ancient evolutionary origins often continue to reduce stomatal initiation at [CO 2 ] levels above current ambient (Kouwenberg et al. 2003; Haworth et al. 2010, 2011a; Grein et al. 2011). ...
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.
Generalised dose–response curves are essential to understand how plants acclimate to atmospheric CO2. We carried out a meta‐analysis of 630 experiments in which C3 plants were experimentally grown at different [CO2] under relatively benign conditions, and derived dose–response curves for 85 phenotypic traits. These curves were characterised by form, plasticity, consistency and reliability. Considered over a range of 200–1200 µmol mol⁻¹ CO2, some traits more than doubled (e.g. area‐based photosynthesis; intrinsic water‐use efficiency), whereas others more than halved (area‐based transpiration). At current atmospheric [CO2], 64% of the total stimulation in biomass over the 200–1200 µmol mol⁻¹ range has already been realised. We also mapped the trait responses of plants to [CO2] against those we have quantified before for light intensity. For most traits, CO2 and light responses were of similar direction. However, some traits (such as reproductive effort) only responded to light, others (such as plant height) only to [CO2], and some traits (such as area‐based transpiration) responded in opposite directions. This synthesis provides a comprehensive picture of plant responses to [CO2] at different integration levels and offers the quantitative dose–response curves that can be used to improve global change simulation models.
Leaf gas exchange is central to the analysis of photosynthetic processes and the development of more productive, water efficient and stress tolerant crops. This has led to a rapid expansion in the use of commercial plant photosynthesis systems which combine infra-red gas analysis and chlorophyll fluorescence (Chl-Flr) capabilities. The present review provides an introduction to the principles, common sources of error, basic measurements and protocols when using these plant photosynthesis systems. We summarise techniques to characterise the physiology of light harvesting, photosynthetic capacity and rates of respiration in the light and dark. The underlying concepts and calculation of mesophyll conductance of CO2 from the intercellular air-space to the carboxylation site within chloroplasts using leaf gas exchange and Chl-Flr are introduced. The analysis of stomatal kinetic responses is also presented, and its significance in terms of stomatal physiological control of photosynthesis that determines plant carbon and water efficiency in response to short-term variations in environmental conditions. These techniques can be utilised in the identification of the irrigation technique most suited to a particular crop, scheduling of water application in precision irrigation, and phenotyping of crops for growth under conditions of drought, temperature extremes, elevated [CO2] or exposure to pollutants.
During the Cretaceous (145-66 Ma), early angiosperms rapidly diversified, eventually outcompeting the ferns and gymnosperms previously dominating most ecosystems. While the cause of their high diversity has been attributed largely to coevolution with pollinators and herbivores, their ability to outcompete the previously dominant ferns and gymnosperms has been the subject of many hypotheses. Common among these is that the angiosperms alone developed leaves with smaller, more numerous stomata and more highly branching venation networks that enable higher rates of transpiration, photosynthesis, and growth. Yet, how angiosperms pack their leaves with smaller, more abundant stomata and more veins is unknown but linked, we show, to simple biophysical constraints on cell size. Here we show that genome downsizing facilitated reductions in cell size necessary to construct leaves with a high density stomata and veins. Rapid genome downsizing during the early Cretaceous allowed angiosperms to push the frontiers of anatomical trait space. In contrast, during the same time period ferns and gymnosperms exhibited no such changes in genome size, stomatal size, or vein density. Further reinforcing the effect of genome downsizing on increased gas exchange rates, we found that species employing water-loss limiting crassulacean acid metabolism (CAM) photosynthesis, have significantly larger genomes than C3 and C4 species. By directly affecting cell size and gas exchange capacity, genome downsizing brought actual primary productivity closer to its maximum potential. These results suggest species with small genomes, exhibiting a larger range of final cell size, can more finely tune their leaf physiology to environmental conditions and inhabit a broader range of habitats.
Selective pressures acting on plant life histories can drive extreme specialization. One example of such specialization is the evolution of dioecious breeding systems. Evolutionary and ecological theory posits that dioecy may subject male and female individuals to different selective pressures and result in unique sex-mediated adaptive traits related to resource allocation and ecophysiology. Cycads are the earliest diverging lineage of seed plants with strict dioecy, yet we know almost nothing about the ecology and physiology of this group. Especially limited is our understanding of potential sex-specific differences and how such differences may influence species ecology. Here we examine the ecophysiology of male and female cycads to understand better, the role that dioecy plays in this group. We evaluated sex-specific differences in ecophysiological traits and resource acquisition in five species. Specifically, we compared photosynthetic physiology, nitrogen and carbon content, isotope discrimination (δ¹⁵N and δ¹³C), and stomatal density. In some cycads, a) males and females have similar investments in leaf nitrogen but females exhibit greater incorporation of nitrogen from nitrogen-fixing soil bacteria, b) males display higher photosynthetic capacity but females show greater water-use efficiency, and c) males have higher stomatal conductance but similar stomatal density to females. This study is the first to examine the ecophysiological differences that have evolved in the oldest dioecious lineage of seed-bearing plants. Our results show unexpected differences in photosynthetic physiology and highlight the co-evolution with nitrogen fixing soil bacteria as a potential new key player in an old lineage.
A negative stable carbon-isotope excursion (CIE) has been identified at sites across the globe in strata that span the Triassic-Jurassic boundary. Different studies have suggested that this negative CIE could be the result of either a change in vegetation or a massive perturbation in the global carbon cycle at this time. To determine which, 84 hand-picked leaf cuticle fragments from plant macrofossils previously identified to genus level were analyzed for stable carbon-isotope values. The samples were taken from known heights in nine plant beds spanning the Rhaetian-Hettangian (Upper Triassic-Lower Jurassic) at AstartekløÃ̧ft, East Greenland. We have constructed taxon-specific stable carbon-isotope curves for Ginkgoales and Bennettitales and compared these to an existing δ 13C curve based on fossil wood from the same section. This study reveals that taxon-specific carbon-isotope curves based on the leaf data from these two seed-plant groups both record the same negative CIE as the fossil wood, despite having different ecological roles and different relative abundances in the section. Correspondence analysis of the macrofossil abundance data, where the plants are considered in their ecological groups, shows that the δ 13C values bear no relationship to changes in vegetation. This result further suggests that vegetation change had little role in determining the δ 13C values at this time. Considered together, the bulk cuticle and taxon-specific δ 13C record indicate that the negative CIE at the Triassic-Jurassic boundary is likely to have been caused by a massive perturbation of the global carbon cycle and not by vegetation change.
Geochemical models of atmospheric evolution predict that during the late Carboniferous, ca. 300 Ma, atmospheric oxygen and carbon dioxide concentrations were 35% and 0.03%, respectively. Both gases compete with eac other for ribulose–1,5–bisphosphate carboxylase/oxygenase–the primary C–fixing enzyme in C3 land plants: and the absolute concentrations and the ratio of the two in the atmosphere have the potential to strongly influenc land–plant function. The Carboniferous therefore represents an era of potentially strong feedback between atmospheric compositio and plant function. We assessed some implications of this ratio of atmospheric gases on plant function using experimenta and modelling approaches. After six weeks growth at 35% O2 and 0.03% carbon dioxide, no photosynthetic acclimation was observed in the woody species Betula pubescens and Hedera helix relative to those plants grown at 21% O2. Leaf photosynthetic rates were 29% lower in the high O2 environment compared to the controls. A global–scale analysis of the impact of the late Carboniferous climate and atmospheri composition on vegetation function was determined by driving a process–based vegetation–biogeochemistry model with a Carboniferou global palaeoclimate simulated by the Universities Global Atmospheric Modelling Programme General Circulation Model. Globa patterns of net primary productivity, leaf area index and soil carbon concentration for the equilibrium model solutions showe generally low values everywhere, compared with the present day, except for a central band in the northern land mass extensio of Gondwana, where high values were predicted. The areas of high soil carbon accumulation closely match the known distributio of late Carboniferous coals. Sensitivity analysis with the model indicated that the increase in O2 concentration from 21% to 35% reduced global net primary productivity by 18.7% or by 6.3 GtC yr–1. Further work is required to collate and map at the global scale the distribution of vegetation types, and evidence for wildfires for the late Carboniferous to test our predictions.
Various aspects of the biochemistry of photosynthetic carbon assimilation in C3 plants are integrated into a form compatible with studies of gas exchange in leaves. These aspects include the kinetic properties of ribulose bisphosphate carboxylase-oxygenase; the requirements of the photosynthetic carbon reduction and photorespiratory carbon oxidation cycles for reduced pyridine nucleotides; the dependence of electron transport on photon flux and the presence of a temperature dependent upper limit to electron transport. The measurements of gas exchange with which the model outputs may be compared include those of the temperature and partial pressure of CO2(p(CO2)) dependencies of quantum yield, the variation of compensation point with temperature and partial pressure of O2(p(O2)), the dependence of net CO2 assimilation rate on p(CO2) and irradiance, and the influence of p(CO2) and irradiance on the temperature dependence of assimilation rate.
Stomatal characteristics of an extinct Cretaceous conifer, Pseudofrenelopsis parceramosa (Fontaine) Watson, are used to reconstruct atmospheric carbon dioxide (pCO2) 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 pCO2 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 pCO2 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 pCO2 values indistinguishable from a soil-carbonate based estimate from the same beds. The new pCO2 estimates are compatible with sedimentological and oxygen-isotope evidence for relatively cool mid-Cretaceous climates.
One of the largest mass extinctions of the past 600 million years (Myr) occurred 200 Myr ago, at the Triassic/Jurassic boundary. The major floral and faunal turnovers have been linked to a marked increase in atmospheric carbon dioxide levels, probably resulting from massive volcanism in the Central Atlantic Magmatic Province. Future climate change predictions suggest that fire activity may increase, in part because higher global temperatures are thought to increase storminess. Here we use palaeontological reconstructions of the fossil flora from East Greenland to assess forest flammability along with records of fossil charcoal preserved in the rocks to show that fire activity increased markedly across the Triassic/Jurassic boundary. We find a fivefold increase in the abundance of fossil charcoal in the earliest Jurassic, which we attribute to a climate-driven shift from a prevalence of broad-leaved taxa to a predominantly narrow-leaved assemblage. Our fire calorimetry experiments show that narrow leaf morphologies are more flammable than broad-leaved morphologies. We suggest that the warming associated with increased atmospheric carbon dioxide levels favoured a dominance of narrow-leaved plants, which, coupled with more frequent lightening strikes, led to an increase in fire activity at the Triassic/Jurassic boundary.
The Carnian flora from Lunz (Lower Austria) ranks among the richest and most diverse fossil floras from the Upper Triassic. It is one of the first modern Triassic floras with bennettitaleans. Although this flora is often referred to in the literature, modern taxonomic studies are mostly absent; only some of the reproductive structures have been studied in detail. Many of the plant remains yield excellently preserved cuticles. During a systematic study of the Pterophyllum leaves from Lunz, it appeared that several species previously accommodated in that taxon have to be transferred to other genera. This paper deals with four species that are transferred to Nilssonia (cycadalean foliage); the macromorphology and epidermal anatomy are described and discussed. The following new combination is introduced: Nilssonia riegeri nov. comb. Two new species are described (i.e. Nilssonia lunzensis and Nilssonia neuberi) based on material originally mentioned in a species list as Ctenis lunzensis Stur nom. nud. and Pterophyllum neuberi Stur nom. nud. The diagnosis for a fourth species, Nilssonia sturii Krasser, is emended. The Nilssonia species from Lunz range among the earliest representatives of the genus Nilssonia.
The hydraulic properties of Pinus pinea, Pinus halepensis and Tetraclinis articulata were studied in a coastal dune area from Eastern Spain. The measured variables include vulnerability to xylem embolism (vulnerability
curves), hydraulic conductivity and carbon isotopic discrimination in leaves. Leaf water potentials were also monitored in
the three studied populations during an extremely dry period. Our results showed that roots had always wider vessels and higher
hydraulic conductivity than branches. Roots were also more vulnerable to xylem embolism and operated closer to their hydraulic
limit (i.e., with narrower safety margins). Although it was not quantified, extensive root mortality was observed in the two
pines during the study period, in agreement with the high values of xylem embolism (> 75%) predicted from vulnerability curves
and the water potentials measured in the field. T. articulata was much more resistant to embolism than P. pinea and P. halepensis. Since T. articulata experienced also lower water potentials, safety margins from hydraulic failure were only slightly wider in this species than
in the pines. Combining species and tissues, high resistance to xylem embolism was associated with low hydraulic conductivity
and with high wood density. Both relationships imply a cost of having a resistant xylem. The study outlined very different
water-use strategies for T. articulata and the pines. Whereas T. articulata had a conservative strategy that relied on the low vulnerability of its conducting system to drought-induced xylem embolism,
the two pines showed regulatory mechanisms at different levels (i.e., embolism, root demography) that constrained the absorption
of water when it became scarce.
pThe majority of the water flux from the earths land surface to the atmosphere passes through the tiny pores (stomata) in the leaves of land plants. The maximum conductance to diffusion of the leaves, determined by the number and geometry of stomata, has a profound effect on the terrestrial water and energy balance. Among tree species, there is ever increasing evidence that anthropogenic increase in atmospheric CO2 concentrations results in a decrease in stomatal frequency. The rate of historical CO2 responsiveness of individual tree species can be used to calibrate empirical models of non-linear (sigmoid) stomatal frequency response to CO2 increase. Modelled response curves for European tree birches (Betula pendula, Betula pubescens) and Durmast oak (Quercus petraea) predict different response limits to CO2 increase (~350 and ~400rppmv, respectively), indicating that non-linear stomatal frequency responses may vary from one tree species to another. Information on a wider selection of species is needed, but the models suggest that the maximum effect of anthropogenic CO2 increase on stomatal frequency has already been reached. Further research is required to establish the effect of rapidly declining response rates on future stomatal conductance of the ecologically contrasting trees of boreal, temperate, subtropical and tropical forests.
Responses of plant leaf stomatal conductance and photosynthesis to water deficit have been extensively reported; however,
little is known concerning the relationships of stomatal density with regard to water status and gas exchange. The responses
of stomatal density to leaf water status were determined, and correlation with specific leaf area (SLA) in a photosynthetic study of a perennial grass, Leymus chinensis, subjected to different soil moisture contents. Moderate water deficits had positive effects on stomatal number, but more
severe deficits led to a reduction, described in a quadratic parabolic curve. The stomatal size obviously decreased with water
deficit, and stomatal density was positively correlated with stomatal conductance (gs), net CO2 assimilation rate (An), and water use efficiency (WUE). A significantly negative correlation of SLA with stomatal density was also observed, suggesting that the balance between leaf area and its matter may be associated with
the guard cell number. The present results indicate that high flexibilities in stomatal density and guard cell size will change
in response to water status, and this process may be closely associated with photosynthesis and water use efficiency.
We investigated the possible effect of recent (1927-1995) increases in the concentration of atmospheric CO2 on the stomatal densities of leaves of a wide range of tree, shrub, and herb species (N = 60) by making new measurements for comparison with corresponding data reported by E. J. Salisbury in 1927--a time when ice core studies indicate CO2 concentrations ~55 mL/L lower than present. A detailed intraspecific study of the herb Mercurialis perennis showed plants of M. perennis in a Cambridgeshire woodland in 1994 had significantly lower stomatal densities, irrespective of leaf insertion point, compared with their 1927 counterparts. Comparisons made across species using evolutionary comparative methods (independent contrasts) revealed a significant (P 2 increases have influenced leaf morphology in a manner consistent with recent experiments and the palaeoecological record. Further analyses suggested that the strength of the stomatal density response was independent of life form but dependent on "exposure" and the initial leaf stomatal density. Consequently, firmer predictions for future changes in stomatal density across all species, expected as a possible result of anthropogenically related CO2 increases, may now be possible.
The species-specific inverse relation between atmospheric CO(2) concentration and stomatal frequency for many woody angiosperm species is being used increasingly with fossil leaves to reconstruct past atmospheric CO(2) levels. To extend our limited knowledge of the responsiveness of conifer needles to CO(2) fluctuations, the stomatal frequency response of four native North American conifer species (Tsuga heterophylla, Picea glauca, Picea mariana, and Larix laricina) to a range of historical CO(2) mixing ratios (290 to 370 ppmV) was analyzed. Because of the specific mode of leaf development and the subsequent stomatal patterning in conifer needles, the stomatal index of these species was not affected by CO(2). In contrast, a new measure of stomatal frequency, based on the number of stomata per millimeter of needle length, decreased significantly with increasing CO(2). For Tsuga heterophylla, the stomatal frequency response to CO(2) changes in the last century is validated through assessment of the influence of other biological and environmental variables. Because of their sensitive response to CO(2), combined with a high preservation capacity, fossil needles of Tsuga heterophylla, Picea glauca, P. mariana, and Larix laricina have great potential for detecting and quantifying past atmospheric CO(2) fluctuations.
Leaf gas exchange characteristics for 16 species of cycad were determined under field conditions in Miami, Fla. Net CO2 assimilation (A(CO2)) ranged from 4.9 μmol · m-2 · s-1 for Lepidozamia peroffskyana Regel to 10.1 μmol · m-2 · s-1 for Zamia furfuracea L. fil. in Aiton. Stomatal conductance to H2O (g(s)) was more variable, ranging from 85 mmol · m-2 · s-1 for Cycas seemannii A. Br. to 335 mmol · m-2 · s-1 for Encephalartos hildebrandtii A. Br. and Bouche. Transpiration (E) ranged from 1.7 mmol · m-2 · s-1 for Cycas chamberlainii W.H. Brown and Keinholz to 4.8 mmol · m-2 · s-1 for Encephalartos hildebrandtii. Highly variable E was more controlling of water-use efficiency than the less-variable A(CO2). The difference between air and pinnae temperature ranged from 0.3 to 1.6 °C and was inversely related to mean g(s) among the species. The values within geographic regions representative of the native habitats of the species were highly variable. For example, two of the African species exhibited the highest and lowest values of water-use efficiency in the survey. Leaf gas exchange for the four largest species with arborescent growth form was less than that for the three small species with subterranean or short bulbous growth form. The diurnal variation in leaf gas exchange for Zamia furfuracea exhibited a two-peaked pattern with a distinct midday depression in A(CO2) and g(s). The ratio dark respiration to maximum A(CO2) for Zamia furfuracea was 0.04. As a group, the values for A(CO2) and g(s) for these cycads ranked at the lower end of the range for all plants species.
The majority of the water flux from the earth's land surface to the atmosphere passes through the tiny pores (stomata) in the leaves of land plants. The maximum conductance to diffusion of the leaves, determined by the number and geometry of stomata, has a profound effect on the terrestrial water and energy balance. Among tree species, there is ever increasing evidence that anthropogenic increase in atmospheric CO2 concentrations results in a decrease in stomatal frequency. The rate of historical CO2 responsiveness of individual tree species can be used to calibrate empirical models of non-linear (sigmoid) stomatal frequency response to CO2 increase. Modelled response curves for European tree birches (Betula pendula, Betula pubescens) and Durmast oak (Quercus petraea) predict different response limits to CO2 increase (∼350 and ∼400 ppmv, respectively), indicating that non-linear stomatal frequency responses may vary from one tree species to another. Information on a wider selection of species is needed, but the models suggest that the maximum effect of anthropogenic CO2 increase on stomatal frequency has already been reached. Further research is required to establish the effect of rapidly declining response rates on future stomatal conductance of the ecologically contrasting trees of boreal, temperate, subtropical and tropical forests.
Stomata1 movement is a manifestation of strain in the epidermis, associated with change in the hydraulic pressure in the epidermal cells. This chapter discusses the role and behavior of stomata in the hydrology of the soil–plant–atmosphere system. Stomata operate in the light in such a way as to maintain positive turgor in the leaves, in the majority of crop plants and other species. The transient response of stomata to changes in environment which cause rapid changes in plant–water relations is quite dramatic. The nature of the stomatal response to change in water potential must involve the mechanical and hydraulic attributes of the stomatal apparatus. There is only a tenuous relationship between the potential of water in leaf tissue in bulk and the local potential of water to which an individual stoma responds in ways, which are also discussed. Thus the transient response of stomata to change in rate of evaporation may be a device which is designed to enhance the speed of the response to light.
The poplar clones Columbia River, Beaupre, Robusta and Raspalje have been investigated in the present (350 μmol mol⁻¹) and double the present (700 μmol mol⁻¹) atmospheric CO2 concentration. Cuttings were planted in pots and were grown in open-top chambers inside a glasshouse for 92 d.
Stomatal density, stomatal index, length of stomatal pore and epidermal cell density were not affected by CO2 enrichment in any of the clones. Lack of differences in stomatal density or index indicate that there were no direct effects of CO2 enrichment on the initiation of the number of stomata during ontogenesis or on epidermal cell expansion at a later stage.
Stomatal conductance decreased because of the effect of CO2 on stomatal opening. The average reduction in both adaxial and abaxial surface has been estimated at 41%. Beaupre showed the largest response of stomatal conductance and Columbia River the smallest.
Stomatal responses to blue and red light were compared in leaves of Xanthium pennsylvanicum (which contain starch in their guard cells) and in onion leaves (which are devoid of starch). Blue light was found to be
more effective than red in opening stomata in both species. However, a significant difference in the ratios of blue to red
light required to produce equal stomatal opening was found between Xanthium pennsylvanicum and onion. It is concluded that blue light may promote stomatal opening by its effect on enzymes controlling the starch and
soluble polysaccharide content of guard cells.
Modifications of the GEOCARBSULF model for Phanerozoic atmospheric oxygen have been made to account for new carbon isotopic data, reconsideration of the fractionation of carbon isotopes between carbonate and organic matter deposited in sediments, and different rates of weathering of volcanic rocks versus granitic rocks. Results indicate distincdy higher O2 values than GEOCARBSULF for the Mesozoic and Cenozoic, lack of an appreciable drop in O 2 below 15 percent at any time, and a small late Cenozoic decline of O2 to the present.
Stomatal density is known to respond to CO2 levels during leaf development. Current interest in the increasing concentration of atmospheric CO2 has stimulated much experimentation on the responses of plants to relatively short-term exposure in artificially high CO2 levels. Attempts to extrapolate from short-term to long-term responses raise fundamental questions concerning evolutionary change in response to rising global CO2 levels. We consider the improved water use efficiency observed under elevated CO2 levels to be the main driving force of natural selection affecting the genotypic component controlling stomatal density. Whether a response is merely phenotypic or becomes incorporated into the genotype depends on two factors: (i) the time scale of exposure and (ii) the generation time of a species. Measurements of stomatal density on fossil leaves of Salix herbacea through a glacial cycle covering the last 140 000 years have shown a decrease in stomatal density in response to the rising CO2 levels of this period. This accords with the shorter-term observations on leaves of trees seen in herbarium specimens where the stomatal density has decreased in response to the rising CO2 levels of the last 200 years. The results indicate that natural selection over the 140000-year period may have favoured a similar response to that shown by trees phenotypically over the last 200 years. Since there is now some evidence for the genetic control of stomatal density, the role of natural selection affecting it must be considered when translating responses from short-term experiments to predict how stomatal density will be affected by long-term climatic and atmospheric change.
Experiments are described in which the responses of wheat stomata to carbon dioxide concentration (0·00, 0·01, 0·02, 0·03 per cent.), light intensity (275, 625, 975 f.c.), and rate of air flow (2, 5, 12·5 l./hr.) were studied.
Reduction of carbon dioxide concentration from 0·03 to 0·01 per cent. resulted in marked stomatal opening; further reduction to 0·00 per cent, was accompanied by a slight but not significant closure. These effects were found at all light intensities and rates of flow, except at 975 f.c. with 2 l./hr. air flow, where no effect of carbon dioxide concentration was detected. This last is attributed to excessive depletion of the carbon dioxide supply by assimilation. The apparent lower limit of 0·01 per cent, carbon dioxide causing maximal stomatal opening is discussed in relation to recent assimilation experiments.
Increase of light intensity caused considerable stomatal opening, this effect being as great with air of 0·00 and 0·01 per cent. as with higher concentrations of carbon dioxide. This suggests an effect of light on stomatal movement other than that exerted indirectly through photosynthesis by the mesophyl cells.
Increased rate of flow of dry air caused closure of the stomata; this was shown to be a drying effect and was absent when moist air was used.
summaryWe investigated interactions between the effects of elevated atmospheric carbon dioxide concentrations ([CO2]) and soil water availability on root biomass, root length and nutrient uptake by spring wheat (Triticum aestivum cv. Tonic). We grew plants at 350 and 700 μmol mol−1 CO2 and with frequent and infrequent watering (‘wet’ and ‘dry’ treatments, respectively). Water use per plant was 1.25 times greater at 350 than at 700 μmol CO2 mol−1, and 1.4 times greater in the ‘wet’ than in the ‘dry’ treatment. Root biomass increased with [CO2] and with watering frequency. Elevated [CO2] changed the vertical distribution of the roots, with a greater stimulation of root growth in the top layers of the soil. These data were confirmed by the video data of root lengths in the ‘dry’ treatment, which showed a delayed root development at depth under elevated [CO2]. The apparent amount of N mineralized appeared to be equal for all treatments. Nutrient uptake was affected by [CO2] and by watering frequency, and there were interactions between these treatments. These interactions were different for N, K and P, which appeared to be related to differences in nutrient availability and mobility in the soil. Moreover, these interactions changed with time as the root system became larger with [CO2] and with watering frequency, and as fluctuations in soil moisture contents increased. Elevated [CO2] affected nutrient uptake in contrasting ways. Potassium uptake appeared to be reduced by the smaller mass flow of water reaching the root surface. However, this might be countered with time by the greater root biomass at elevated [CO2], by the greater soil moisture contents at elevated [CO2], enabling faster diffusion, or both. Phosphorus uptake appeared to be increased by the greater root biomass at elevated [COJ. We conclude that plant nutrient uptake at elevated [CO2] is affected by interactions with water availability, though differences between nutrients preclude generalizations of the response.
Nothofagus cunninghamii
(Hook.) Oerst. clones of four different genotypes from Mt Field National Park,
Tasmania were grown at both current (~370 mol
mol–1 ) and depleted (~170 mol mol
–1 ) CO2. Growth was
significantly less in the lower [CO2]
treatment in all genotypes. The amount of growth reduction caused by low
[CO2] depended strongly upon genotype and
varied from less than 30% to greater than 75% reduction of whole
plant biomass when compared to growth at current
[CO2]. Specific leaf area was significantly
greater in all plants grown in reduced [CO2],
whereas individual leaf area was not significantly affected by
[CO2]. The direction and magnitude of the
response of stomatal index, stomatal density and epidermal cell density to
[CO2] was strongly dependent upon genotype.
[CO2] had a significant effect on the length
of the stomatal pore, but the magnitude of the effect (~3%) was trivial
compared to changes in stomatal density (up to 20%). There was a
significant (P < 0.01) and positive relationship between the response of
stomatal density and growth response of a genotype. Therefore, we propose that
the response of stomatal density to [CO2]
controls the relative growth response of N. cunninghamii
and that this response is highly dependent upon genotype.
Gas exchange measurements were made on saplings of Southern Beech,
Nothofagus cunninghamii (Hook.) Oerst. collected from
three altitudes (350, 780 and 1100 m above sea level) and grown in a common
glasshouse trial. Plants were grown from cuttings taken 2 years earlier from a
number of plants at each altitude in Mt Field National Park, Tasmania.
Stomatal density increased with increasing altitude of origin, and stomatal
con-ductance and carbon assimilation rate were linearly related across all
samples. The altitude of origin influenced thestomatal conductance and
therefore carbon assimilation rate, with plants from 780 m having a greater
photosynthetic rate than those from 350 m. The intercellular concentration of
CO2 as a ratio of external CO2
concentration
(ci/ca)
was similar in all plants despite the large variation in maximum stomatal
conductance. Carboxylation efficiency was greater in plants from 780 m than in
plants from 350 m. Altitude of origin has a strong influence on the
photo-synthetic performance of N. cunninghamii plants
even when grown under controlled conditions, and this influence is expressed
in both leaf biochemistry (carboxylation efficiency) and leaf morphology
(stomatal density).
Experiments on a range of species of tree, shrub and herb have shown that stomatal density and stomatal index increase as the partial pressure of CO2 decreases over the range from the current level of 34 Pa to 22.5 Pa. Stomatal density responds to the reduced partial pressure of CO2 in a simulation of high altitude (3000 m), when the CO2 mole fraction is unchanged.
When the partial pressure of CO2 is increased from 35 to 70 Pa stomatal density decreases slightly, with a response to unit change in CO2 which is about 10% of that below 34 Pa.
Measurements of gas exchange on leaves which had developed in different CO2 partial pressures, but at low saturation vapour pressure deficits in the range of 0.7 to 0.9 kPa, indicated lower photosynthetic rates but higher stomatal conductances at reduced CO2 partial pressures.
Experiments on populations of Nardus stricta originating from altitudes of 366 m and 810 m in Scotland, indicated genetic differences in the responses of stomatal density to CO2 in pressures simulating altitudes of sea level and 2 000 m. Plants from the higher altitude showed greater declines in stomatal density when the CO2 partial pressure was increased.
Stomatal opening in Xanthium pennsylvanicum was found to be significantly greater in blue light than in red. Experiments in which leaves were placed in a closed system
and allowed to establish their own steady-state carbon dioxide concentration showed that when the CO2 concentration was about the same as that in red, opening was much greater in blue light. Blue light of low intensity could
cause as great an opening as red of higher intensity, even though the CO2 concentration was much higher in blue. Stomatal opening in light is considered as involving at least two reactions: (1) a
response to the removal of CO2 by photosynthesis; (2) a response to blue light not dependent on the removal of CO2.
Blue light became increasingly effective, relative to red, as the length of night was increased over the range 2 to 14 hours.
This might, in part, explain previously observed effects of night length on rate of opening in light.
The initial very rapid phase of closure in darkness appeared to be independent of CO2 accumulation, for it was not prevented by flushing the intercellular spaces with air free of CO2. It is suggested that closure in darkness, like opening in light, should be considered as involving components both dependent
upon, and independent of, CO2 concentration.
A survey of 100 species and 122 observations has shown an average reduction in stomatal density of 14.3% (SE ±2.2 %) with CO 2 enrichment, with 74% of the cases exhibiting a reduction in stomatal density. A sign test demonstrated that stomatal density decreases, in response to CO 2 , significantly more often than expected by chance. Repeated observations on the same species indicated a significant repeatability in the direction of the stomatal response. Analyses which removed the potential effect of taxonomy on this data set showed no significant patterns in the dependency of the degree of stomatal change on growth form (woodiness vs. non‐woodiness; trees vs. shrubs), habitat (cool vs. warm) or stomatal distribution on the leaf (amphi‐ vs. hypostomatous).
Forty‐three of the observations had been made in controlled environments and under a typical range in CO., enrichment of 350–700 μmol mol ⁻¹ . For these cases the average stomatal density declined by 9% (SE ± 3.3%) and 60% of the cases showed reductions in stomatal density. When analyses were restricted to these 43 observations, amphistomatous samples more frequently had greater changes in stomatal density than did hypostomatous samples.
The degree of reduction in stomatal density with increasing CO 2 increases with initial stomatal density, after the influence of taxonomy is removed using analyses of independent contrasts. When the data were examined for patterns that might be due explicitly to the effects of relatedness, the subclasses of the Hamamelidae and the Rosidae showed highly significant reductions in stomatal density with CO 2 (87% of the species studied in the Hamamelidae and 80% of the species in the Rosidae showed reduction with CO 2 enrichment) and correlations between initial stomatal density and degree of reduction in stomatal density. The species sampled in the Hamamelidae were dominantly trees, whereas herbs dominated the species in the Rosidae. There were insufficient species studied at lower taxonomic levels to warrant further statistical analyses. This problem results from experimental and observational data being most often restricted to one species per taxonomic level, typically up to the level of order, a feature which can severely limit the extraction of taxonomically‐related and ecologically‐related plant responses.
Available evidence seems to indicate that the earliest cycads and cycadeoids were slender plants, without a persistent armor of leaf bases and often with small leaves. One prevailing viewpoint is that earliest cycads had entire leaves, and that pinnation was a derived state, coming about by progressive incising of a taeniopterid leaf. An alternative suggestion is presented here, proposing that a dissected leaf could have been a primitive one for cycads, and that occurrence of pinnately compound cycad or cycad-like leaves in the Triassic Period may be interpreted as a manifestation of this early dissected state. It is further proposed that the primitive cycad megasporophyll need not have been one with a taeniopterid distal lamina, but one derived from a dissected leaf. Tinsleya texana is suggested as representing a possible ancestral state. The absence of compelling evidence to support any single viewpoint permits the proposing of more than one hypothesis.
Estimates of pCO2 for the early Paleogene vary widely, from near modern-day levels to an order of magnitude greater, based on various proxy measures. Resolving the relationship between climate and pCO2 during this globally warm period is a key task in understanding climate dynamics in a warmer world. Here, we use the stomatal frequency of fossil Ginkgo adiantoides from the Okanagan Highlands of British Columbia, Canada to estimate pCO2 during the Early Eocene Climatic Optimum (EECO), the interval of peak warmth in the Cenozoic. We also examine a dataset of modern Ginkgo biloba leaves to critically assess the accuracy and precision of stomatal frequency as a proxy indicator of pCO2. Early Eocene fossil G. adiantoides has significantly lower stomatal frequency than modern G. biloba, suggesting pCO2 levels >2× modern pre-industrial values. This result is in contrast to earlier studies using stomatal frequency of Ginkgo that indicated near modern-day levels of pCO2 in the early Paleogene, though not including samples from the EECO. We also find that levels of pCO2 as indicated by stomatal frequency are correlated with trends in climate (mean annual temperature) over time at the Falkland fossil locality, suggesting that climate and pCO2 were coupled during the EECO hyperthermal.
Stomatal frequency of fossil conifers and ginkgoals cuticles were considered as potential indicators of the pCO2 values in the Patagonian palaeoatmosphere during the Cretaceous. Samples are from continental deposits of early Upper Aptian age (Anfiteatro de Ticó and Punta del Barco formations) and Upper Albian–Lower Cenomanian age (Kachaike Formation), both outcropping in Andean and extra-Andean portions of Santa Cruz province, Argentina. It can be inferred that the CO2 atmospheric content was similar during both stages, or was slightly higher toward the Late Albian–Early Cenomanian. The CO2 content estimated from the conifers is between ~700 and 1400 ppmv (or lower from the mid-Aptian ginkgoals). This CO2 range is consistent with those predicted worldwide by previous studies (stomatal indices, biogeochemical models and carbon isotopes), and implies a CO2 content 2.3–4.0 times higher than present. The high atmospheric CO2 content during the Middle Aptian and Late Albian–Early Cenomanian was probably linked to a warming process at high latitudes during these times. This is consistent with the floristic development recorded during both stages in Patagonia.
In flowering plants, genes have frequently been transferred from mitochondria to the cell nucleus by way of a remarkable evolutionary rapid-transit system.
Experiments are described in which the responses of wheat stomata to carbon dioxide concentration (0·00, 0·01, 0·02, 0·03 per cent.), light intensity (275, 625, 975 f.c.), and rate of air flow (2, 5, 12·5 l./hr.) were studied.Reduction of carbon dioxide concentration from 0·03 to 0·01 per cent. resulted in marked stomatal opening; further reduction to 0·00 per cent, was accompanied by a slight but not significant closure. These effects were found at all light intensities and rates of flow, except at 975 f.c. with 2 l./hr. air flow, where no effect of carbon dioxide concentration was detected. This last is attributed to excessive depletion of the carbon dioxide supply by assimilation. The apparent lower limit of 0·01 per cent, carbon dioxide causing maximal stomatal opening is discussed in relation to recent assimilation experiments.Increase of light intensity caused considerable stomatal opening, this effect being as great with air of 0·00 and 0·01 per cent. as with higher concentrations of carbon dioxide. This suggests an effect of light on stomatal movement other than that exerted indirectly through photosynthesis by the mesophyl cells.Increased rate of flow of dry air caused closure of the stomata; this was shown to be a drying effect and was absent when moist air was used.
The abundance of transcripts of cab-7 and cab-3C, which code for the chlorophyll a/b binding proteins of the light-harvesting complexes I and II, respectively, and the abundance of transcripts of Rca, which encodes Rubisco activase, were reduced in tomato plants exposed to high CO2 for up to 9d, whereas the abundance of mRNA from psa A–psa B and psb A, which encode the proteins of the core complex of PSI and the D1 protein of PSII, respectively, and the abundance of glycolate oxidase, which is involved in photorespiration, were not affected. However, the abundance of the transcript for the B subunit of ADP-glucose pyrophosphorylase was increased after 1 d at elevated CO2. The chlorophyll a/b ratio decreased significantly over 9 d of exposure to elevated CO2. The responses of the nuclear genes to high CO2 were enhanced when leaves were detached so as to deprive them of any major sink. The responses of these transcripts to high CO2 were mimicked when sucrose or glucose was supplied to the leaf tissue, whereas acetate or sorbitol had no effect. Carbohydrate analyses of leaves grown in high CO2 or supplied with sucrose revealed that major increases occurred in the amount of glucose and fructose.
Based on these and other published data, a molecular model involving the repression or activation of the transcription of nuclear genes coding for chloroplast proteins by photosynthetic end-products is proposed to account for photosynthetic acclimation to high CO2 in tomato plants and other species.
Neogene atmospheric paleo-CO 2 estimates based on fossils of the extant cupressaceous conifer species Taxodium distichum from the Brandywine Formation of Maryland and the Citronelle Formation of southern Alabama are presented. These are important as the first such estimates from eastern North American paleofloras, and provide new evidence from a time for which the role of CO 2 in climate change is controversial. Comparisons of the stomatal density (SD) of the fossil leaf cuticles to a calibration curve constructed from modern leaves of the same species collected over the last century of anthropogenic CO 2 increase produces Miocene and Pliocene atmospheric paleo-CO 2 mean estimates of 360 and 351 ppmv, respectively. Although the temporal resolution of the fossil sites is low, these results are in agreement with multiple independent proxies that indicate near modern CO 2 levels during this interval, and demonstrate the utility of T. distichum leaves as instruments for stomatal frequency analysis.
The record of Cycadales in Patagonia begins in the Triassic and extends up to the Oligocene. In this region the group is highly diversified and includes several taxa represented by trunks, leaves and pollen cones. A new cycadalean genus and species, Restrepophyllum chiguoides, form the Aptian Anfiteatro de Ticó Formation, Santa Cruz province, Argentina, is described here. The fossil is a leaf compression with well-preserved cuticle. Its morphology, anatomy and ultrastructure are studied by means of light and electron microscopy. The leaf is lanceolate, serrate, and possesses a prominent midvein and decurrent laterals showing an open, simple or dichotomous venation. The leaf is hypostomatic, and the abaxial cuticle is thinner than the adaxial one. The stomata are irregularly distributed and indistinctly oriented between veins. They are monocyclic to imperfectly dicyclic (haplocheilic); the suprastomatal aperture is raised over the epidermis and the guard cells are sunken. Scattered trichomes and crystalliferous idioblasts are also present. The cuticle is composed of three layers: the outer and inner layers are lamellate, while the middle one is granulate. This new cycad leaf is compared with similar fossil leaves from Gondwana and Europe/North America, and also with similar extant cycad leaves. Based on the general morphology and the main characters of the cuticle, R. chiguoides is assigned to the family Zamiaceae; moreover it is more closely related to the living Zamia (Chigua) restrepoi (D. Stevenson) Lindstrom than to any other member of the Cycadales. Paleophytogeographic evidence suggests a South American origin of Zamia/Chigua and a further migration to northern latitudes. This new type of leaf also suggests the putative existence of a Chigua clade that may be traced back to the Early Cretaceous when two cycadalean families, Zamiaceae and Stangeriaceae, were already well-established in Patagonia.
Ambient atmospheric CO2 concentration ([CO2]a) has apparently declined from values above 200μmol mol−1 to values below 200μmol mol−1 within the last several million years. The lower end of this range is marginal for C3 plants. I hypothesize that: (1) declining [CO2]a imposed a physiological strain on plants, and plant taxa evolving under declining [CO2]a tended to develop compensating mechanisms, including increased stomatal efficiency; (2) angiosperms were better able to adjust to declining [CO2]a than were gymnosperms and pteridophytes; and (3) angiosperm adjustment has been uneven. Fast-evolving taxa (e.g. grasses and herbs) have been better able to adapt to CO2 starvation. If these propositions are true, stomatal adjustment mechanisms should show patterned variation, and a single pattern of stomatal regulation cannot be assumed.
Background and Aims: Leaf stomatal density, i.e. number of stomata per unit area of leaf, is a primary determinant of the carbon and water relations of plants. However, little is known about the plasticity of grapevine stomatal density during leaf formation in response to environmental factors. In this study, we determined responses in stomatal density to soil temperature and atmospheric carbon dioxide during leaf development following dormancy to gain further understanding of grapevine carbon and water relations, and adaptation to climate change.
Methods and Results: Using potted plants of Vitis vinifera (L.) cv. Chardonnay, we found that a period of soil warming from budbreak reduced stomatal density of concurrently formed leaves, whereas CO2 depletion increased it. Furthermore, stomatal density of concurrently formed leaves was closely and inversely correlated with starch concentration in roots and trunks.
Conclusion: We conclude that the stomatal density of grapevine leaves varies greatly in response to soil temperature and atmospheric CO2 concentration.
Significance of the Study: This is the first study to show that soil temperature influences stomatal density of plants. It also confirms that stomatal density of grapevines, like many other plants, responds inversely to atmospheric CO2 concentration. Our findings demonstrate that stomatal density must be accounted for in any attempt to predict grapevine adaptation to climate change, and attendant impacts on CO2 assimilation and water use efficiency in viticulture. More fundamentally, they indicate that the carbohydrate reserve status of perennial, deciduous plant species may be an important endogenous determinant of stomatal density.
The ability of a plant to survive severe water deficits depends on its ability to restrict water loss through the leaf epidermis after stomata attain minimum aperture. At this stage, the rate of water loss is regulated by the epidermal conductance (gc). Low gc would be a useful selection criterion to identify genotypes with enhanced survival capability. Consequently, variation in gc among Sorghum bicolor (L.) Moench genotypes was evaluated. Since there is little conclusive evidence linking gc with leaf waxiness, alternative hypotheses relating gc to stomatal trails were also examined. Epidermal conductance varied from 6.3 to 17.6mmol m−2 s−1 among sorghum genotypes. It was unrelated to stomatal pore length which varied with genotype and to pore depth which was similar for all genotypes measured. However, gc, increased with increasing stomatal density. This indicates that stomatal density plays a direct role in water loss even at very low conductances. The association of low stomatal density with low gc is consistent with the hypothesis that at the smallest stomata aperture, water loss from the epidermis above guard cell teichodes becomes a significant source of leaf water loss. Since low gc is directly related to crop survival under severe water deficits, it is recommended that genotypes with low gc. be selected using the selection criterion of stomatal density.
Stomatal density is known to respond to CO2 levels during leaf development. Current interest in the increasing concentration of atmospheric CO2 has stimulated much experimentation on the responses of plants to relatively short-term exposure in artificially high CO2 levels. Attempts to extrapolate from short-term to long-term responses raise fundamental questions concerning evolutionary change in response to rising global CO2 levels. We consider the improved water use efficiency observed under elevated CO2 levels to be the main driving force of natural selection affecting the genotypic component controlling stomatal density. Whether a response is merely phenotypic or becomes incorporated into the genotype depends on two factors: (i) the time scale of exposure and (ii) the generation time of a species. Measurements of stomatal density on fossil leaves of Salix herbacea through a glacial cycle covering the last 140000 years have shown a decrease in stomatal density in response to the rising CO2 levels of this period. This accords with the shorter-term observations on leaves of trees seen in herbarium specimens where the stomatal density has decreased in response to the rising CO2 levels of the last 200 years. The results indicate that natural selection over the 140000-year period may have favoured a similar response to that shown by trees phenotypically over the last 200 years. Since there is now some evidence for the genetic control of stomatal density, the role of natural selection affecting it must be considered when translating responses from short-term experiments to predict how stomatal density will be affected by long-term climatic and atmospheric change.
Major fluctuations in the concentrations of atmospheric CO2 and O2, are predicted by historical long-term carbon and oxygen cycle models of atmospheric evolution and will have impacted directly on past climates, plant function and evolutionary processes. Here, palaeobotanical evidence is presented from the stomatal density record of fossil leaves spanning the past 400 Myr supporting the predicted changes in atsmopheric CO2. Evidence from experiments on plants exposed to long-term high CO2, environments and the newly-assembled fossil data indicate the potential for genetic modification of stomatal characters. The influence of the changes in fossil stomatal characteristics and atmospheric composition on the rates of leaf gas exchange over the course of land plant evolution has been investigated through modelling. Three contrasting eras of plain water economics emerge in the Devonian (high), Carboniferous (low) and from the Upper Jurassic to the present-day (high but declining). These patterns of change result from structural changes of the leaves and the impact of atmospheric CO2, and O2, concentrations on RuBisCo function and are consistent with the fossil evidence of sequential appearances of novel plant anatomical changes. The modelling approach is tested by comparing predicted leaf stable carbon isotope ratios with those measured on fossil plant and organic material. Viewed in a geological context, current and future increases in the concentration of atmospheric CO2, might be considered as restoring plant function to that more typically experienced by plants over the majority of their evolutionary history.
Three new species of the cycadean pollen cone Androstrobus, viz. A. munku, A. patagonicus, and A. rayen, are described. All specimens are represented by microsprophylls or fragmentary cone pieces, and they have been found in the same fossil bed at the locality Bajo Grande, in Santa Cruz province, Argentina, which is referred to the Anfiteatro de Ticó Formation of Aptian age. This is the first record of the genus in Argentina and South America. The good preservation of the material allowed the study of cuticles and pollen with scanning electron microscopy (SEM) and transmission electron microscopy (TEM). It is noted that Androstrobus is a poorly defined genus that needs a revision of the type material as well as new specimens from the type locality to certify the presence of pollen. Comparisons with other Androstrobus species are made, especially with those that have been described with cuticular characters and structure of pollen. Attention is paid to the similarity of the alveolate pollen ultrastructure of the Patagonian fossils with some extant cycads, especially with genera of the Zamiaceae and Cycadaceae. The variety of pollen cones found in the same bed agrees with the presence of different vegetative organs, leaves, and fronds found previously at the same place, and that were referred to the cycads on the base of their cuticular structure. The abundance of cycads during the mid-Cretaceous in southern Argentina is a contrasting evidence with the present-day absence of the group in southern South America.
Summary • Leaf morphology varies predictably with altitude, and leaf morphological features have been used to estimate average temperatures from fossil leaves. The altitude–leaf morphology relationship is confounded by the two processes of acclimation and adaptation, which reflect environmental and genetic influences, respectively. • Here we describe the relationship between altitude and leaf morphology for Southern beech, Nothofagus cunninghamii (Hook.) Oerst.. Cuttings from several trees from each of four altitudes were grown in a common glasshouse experiment, and leaf morphology related to both genotype and altitude of origin. • Genotype had a significant impact on leaf morphology, but in the field there was also a significant, overriding effect of altitude. This altitude effect disappeared in glasshouse-grown plants for all morphological variables other than leaf thickness and specific leaf area. • These results show that, while leaf length, width and area are partially controlled by genetic factors, these variables are plastic and respond to environmental influences associated with a particular altitude. Thus altitudinal trends in leaf size in N. cunninghamii are unlikely to be the result of adaptation.
This paper describes a new approach to the calibration of thermal infrared measurements of leaf temperature for the estimation of stomatal conductance and illustrates its application to thermal imaging of plant leaves. The approach is based on a simple reformulation of the leaf energy balance equation that makes use of temperature measurements on reference surfaces of known conductance to water vapour. The use of reference surfaces is an alternative to the accurate measurement of all components of the leaf energy balance and is of potentially wide application in studies of stomatal behaviour. The resolution of the technique when applied to thermal images is evaluated and some results of using the approach in the laboratory for the study of stomatal behaviour in leaves of Phaseolus vulgaris L. are presented. Conductances calculated from infrared measurements were well correlated with estimates obtained using a diffusion porometer.
Wood density (D
t), an excellent predictor of mechanical properties, is typically viewed in relation to support against gravity, wind, snow, and other environmental forces. In contrast, we show the surprising extent to which variation in D
t and wood structure is linked to support against implosion by negative pressure in the xylem pipeline. The more drought-tolerant the plant, the more negative the xylem pressure can become without cavitation, and the greater the internal load on the xylem conduit walls. Accordingly, D
t was correlated with cavitation resistance. This trend was consistent with the maintenance of a safety factor from implosion by negative pressure: conduit wall span (b) and thickness (t) scaled so that (t/b)2 was proportional to cavitation resistance as required to avoid wall collapse. Unexpectedly, trends in D
t may be as much or more related to support of the xylem pipeline as to support of the plant.
End-Triassic fluctuations in atmospheric carbon dioxide (CO2) concentration were reconstructed by the use of stomatal frequency analysis on a single plant species: the seedfern Lepidopteris ottonis (Goeppert) Schimper. Stomatal index showed no distinct intra- and interpinnule variation which makes it a suitable proxy for past relative CO2 changes. Records of decreasing stomatal index and density from the bottom to the top of the Rhaetian–Hettangian Wüstenwelsberg section (Bavaria, Germany) indicate rising CO2 levels during the Triassic–Jurassic transition. Additionally, stomatal frequency data of fossil ginkgoalean leaves (Ginkgoites taeniatus (Braun) Harris) suggest a maximum palaeoatmospheric CO2 concentration of 2750 ppmv for the latest Triassic.
A model for the combined long-term cycles of carbon and sulfur has been constructed which combines all the factors modifying weathering and degassing of the GEOCARB III model [Berner R.A., Kothavala Z., 2001. GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. Am. J. Sci. 301, 182–204] for CO2 with rapid recycling and oxygen dependent carbon and sulfur isotope fractionation of an isotope mass balance model for O2 [Berner R.A., 2001. Modeling atmospheric O2 over Phanerozoic time. Geochim. Cosmochim. Acta65, 685–694]. New isotopic data for both carbon and sulfur are used and new feedbacks are created by combining the models. Sensitivity analysis is done by determining (1) the effect on weathering rates of using rapid recycling (rapid recycling treats carbon and sulfur weathering in terms of young rapidly weathering rocks and older more slowly weathering rocks); (2) the effect on O2 of using different initial starting conditions; (3) the effect on O2 of using different data for carbon isotope fractionation during photosynthesis and alternative values of oceanic δ13C for the past 200 million years; (4) the effect on sulfur isotope fractionation and on O2 of varying the size of O2 feedback during sedimentary pyrite formation; (5) the effect on O2 of varying the dependence of organic matter and pyrite weathering on tectonic uplift plus erosion, and the degree of exposure of coastal lands by sea level change; (6) the effect on CO2 of adding the variability of volcanic rock weathering over time [Berner, R.A., 2006. Inclusion of the weathering of volcanic rocks in the GEOCARBSULF model. Am. J. Sci.306 (in press)]. Results show a similar trend of atmospheric CO2 over the Phanerozoic to the results of GEOCARB III, but with some differences during the early Paleozoic and, for variable volcanic rock weathering, lower CO2 values during the Mesozoic. Atmospheric oxygen shows a major broad late Paleozoic peak with a maximum value of about 30% O2 in the Permian, a secondary less-broad peak centered near the Silurian/Devonian boundary, variation between 15% and 20% O2 during the Cambrian and Ordovician, a very sharp drop from 30% to 15% O2 at the Permo-Triassic boundary, and a more-or less continuous rise in O2 from the late Triassic to the present.
Detailed anatomical studies on leaves of Quercus petraea enable the recognition of distinct sun and shade morphotypes based on epidermal and mesophyll characteristics. Epidermal cell properties, like the cell area and the corresponding epidermal cell density, the anticlinal wall undulation and the structure of the palisade parenchyma are good parameters to differentiate between sun and shade leaves. These distinguishing leaf anatomical characteristics also reveal distinct sun and shade morphotypes among 50 leaf remains of Q. pseudocastanea, the fossil representative of Q. petraea, from two Late Miocene clay intercalations in the open-cast mine Hambach (Germany). Like their recent equivalents, fossil sun morphotypes show higher epidermal density as a result of a restricted amount of lateral epidermal cell expansion. Correspondingly, the stomatal density in sun leaves is considerably increased by about 60%, whereas the stomatal index is only slightly higher. Fossil sun leaves are also characterized by straight to rounded epidermal cell walls and a thicker palisade parenchyma due to a second cell layer. Fossil shade leaves in turn show a pronounced undulation of the epidermal cell walls and only a single layered-palisade parenchyma. The rich fossil oak leaf assemblages are characterized by a high abundance (90%) of sun morphotypes, which is mainly the result of taphonomic processes. This remarkable predominance of sun morphotypes evokes a confident reproducibility of former analysis of stomatal parameters as a measure of palaeoatmospheric CO2 levels. However, the stomatal density with its high variability should only be used as a bioindicator of palaeoatmospheric CO2 levels in large data sets or from one particular leaf morphotype, preferably from sun leaves. In the case of small sample sets, the application of the stomatal index is highly recommended.