Tree-ring analysis and conifer growth responses to increased atmospheric CO2 levels

Summary Tree-ring data of naturally grown connifers were analyzed to evaluate the possibility of enhanced tree growth due to increased atmospheric CO₂. Tree cores were obtained from 34 sites in four different climatic regions in the northern hemisphere. In each of the four regions, the sampling sites were located along ecological gradients between the subalpine treeline and low elevations and, sometimes, the arid forest border. Growth trends after 1950, when the atmospheric CO₂ concentration increased by more than 30 l·l^-1 indicate an increase in ring-widths at eight of the 34 sites. These chronologies were from sites which moderate temperature or water stress. In four cases the growth increase in the post-1950 period coincided with favorable climatic conditions. In the remaining four cases, the growth increase exceeded the upper bound response expected from CO₂ enrichment experiments with seedling conifer species. Therefore, increased growth in any of the tree-ring chronologies examined could not be solely attributed to higher atmospheric CO₂ concentrations.Major financial supporters: Swiss National Science Foundation (application no. 1.869-0.83); Swiss Federal Institute of Forestry Research, 8903 Birmensdorf, Switzerland; other financial supporters: Carbon Dioxide Research Division, U.S. Department of Energy under subcontract no. 11X-57507V with Martin Marietta Energy Systems, IncOperated by Martin Marietta Energy Systems, Inc., under contract DE-AC05-840R21400 with U.S. Department of Energy     

Stomatal density and aperture length in four plant species grown across a subambient CO2 gradient

Stomatal density, stomatal aperture length, area/leaf, and number of stomata/leaf were measured after the annual C₃ agronomic grasses oats (Avena sativa) and wheat (Triticum aestivum), the C, woody legume honey mesquite (Prosopis glandulosa), and the perennial C₄ grass little bluestem (Schizachyrium scoparium) were grown across a subambient carbon dioxide concentration ([CO₂]) gradient from near 200 to 350 μmol/mol in a growth chamber. The purpose was to determine if the size and density of stomata vary in response to atmospheric [CO₂] during growth, across a subambient [CO₂] range representative of the doubling that has occurred since the last ice age. Changes in stomatal density and aperture length with increasing [CO₂] were small when detected. Stomatal density decreased on adaxial flag leaf surfaces of wheat, and aperture length increased slightly with [CO₂], Leaf area and number of stomata/flag leaf increased by similar proportions with [CO₂] in two wheat cultivars. No consistent relationship between [CO₂] and stomatal density or size was detected in mesquite, oats, or little bluestem. We conclude that individual plants of these species lack the plasticity to significantly alter stomatal density and aperture length in response to increasing atmospheric [CO₂] in a single generation (annuals) or growing season (perennials).     

Short communication. Stomatal responses of the 'living fossil' Ginkgo biloba L. to changes in atmospheric CO2 concentrations

Leaf stomatal density and index of Ginkgo biloba L. were both significantly (P<0.05) reduced after 3 years growth at elevated CO2 (560 ppm), with values comparable to those of cuticles prepared from Triassic and Jurassic fossil Ginkgo leaves thought to have developed in the high CO2 'greenhouse world' of the Mesozoic. A reciprocal transfer experiment indicated that reductions in stomatal density and index irreversibly reduced stomatal conductance, particularly at low leaf-to-air vapour pressure deficits and low internal leaf CO2 concentrations (Ci). These effects probably contributed to the high water-use efficiency of Ginkgo spp. in the Mesozoic relative to those of the present, as determined from carbon isotope measurements of extant and fossil cuticles.Keywords: Stomata, gas exchange, elevated CO2, fossils.      

Stomatal density and aperture in non-vascular land plants are non-responsive to above-ambient atmospheric CO2 concentrations

Background and Aims 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.Methods 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.Key Results 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].Conclusions 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.     

Stomatal responses to changes in atmospheric humidity and water supply: Experiments with leaf sections of Zea mays in CO2-free air

Summary Leaf sections were exposed to CO₂-free air, thus excluding interference by the CO₂-sensitive system in the guard cells. Stomates did not close in response to change from moist to dry air, whether it passed over the leaf or was forced through the intercelluar spaces. In contrast, the stomatal apertures became narrower if the water potential in the liquid supplying the leaf was lowered. Of solutions with the same osmolality, those with the higher viscosity produced the larger responses.Transient stomatal movements in the opposite direction to the final response were observed upon any sudden change in the water status of the leaf sections, whether caused by varying the moisture content of the air passing around or through the leaf sections, or by varying the water supply. Increased load on the water supply caused temporary opening movements, while improvements in water supply led to closing movements of varying duration. When dry air was forced through the leaf sections, non-sinusoidal oscillations with large amplitudes were sometimes observed.It is concluded that the guard cells are tightly coupled to the water-supply system of the leaf and only indirectly to the conditions in the atmosphere by a negative feedback of transpiration on the water potential in the water-conducting system.     

High altitude acclimatization in plants: Stomatal frequency and anatomical changes in leaves ofArtemisia species

During high altitude acclimatization both the number of stomata and their pore width decreased. The number of open stomata per unit leaf area in the morning and evening hours was higher as compared to that in plants grown at a lower altitude. Thickness of leaves also decreased at high altitudes but the effect on the size of epidermal, mesophyll and spongy parenchymatous cells varied from species to species. Adaptational significance of these changes are discussed. This work was supported through a grant to the second author by Department of Science and Technology (SERC) Govt. of India.     

Differential anatomical responses to elevated CO2 in saplings of four hardwood species

To determine whether an elevated carbon dioxide concentration ([CO₂]) can induce changes in the wood structure and stem radial growth in forest trees, we investigated the anatomical features of conduit cells and cambial activity in 4‐year‐old saplings of four deciduous broadleaved tree species – two ring‐porous (Quercus mongolica and Kalopanax septemlobus) and two diffuse‐porous species (Betula maximowicziana and Acer mono) – grown for three growing seasons in a free‐air CO₂ enrichment system. Elevated [CO₂] had no effects on vessels, growth and physiological traits of Q. mongolica, whereas tree height, photosynthesis and vessel area tended to increase in K. septemlobus. No effects of [CO₂] on growth, physiological traits and vessels were seen in the two diffuse‐porous woods. Elevated [CO₂] increased larger vessels in all species, except B. maximowicziana and number of cambial cells in two ring‐porous species. Our results showed that the vessel anatomy and radial stem growth of Q. mongolica, B. maximowicziana and A. mono were not affected by elevated [CO₂], although vessel size frequency and cambial activity in Q. mongolica were altered. In contrast, changes in vessel anatomy and cambial activity were induced by elevated [CO₂] in K. septemlobus. The different responses to elevated [CO₂] suggest that the sensitivity of forest trees to CO₂ is species dependent.     

Stomatal Responses of Variegated Leaves to CO2 Enrichment

The responses of stomatal density and stomatal index of fivespecies of ornamental plants with variegated leaves grown attwo mole fractions of atmospheric CO₂ (350 and 700 µmolmol^-1) were measured. The use of variegated leaves allowed anypotential effects of mesophyll photosynthetic capacity to beuncoupled from the responses of stomatal density to changesin atmospheric CO₂ concentration. There was a decrease in stomataldensity and stomatal index with CO₂ enrichment on both white(unpigmented) and green (pigmented) leaf areas. A similar responseof stomatal density and index was also observed on areas ofleaves with pigmentation other than green indicating that anydifferences in metabolic processes associated with colouredleaves are not influencing the responses of stomatal densityto CO₂ concentrations. Therefore the carboxylation capacityof mesophyll tissue has no direct influence on stomatal densityand index responses as suggested previously (Friend and Woodward1990 Advances in Ecological Research 20: 59-124), instead theresponses were related to leaf structure. The stomatal characteristics(density and index) of homobaric variegated leaves showed agreater sensitivity to CO₂ on green portions, whereas heterobaricleaves showed a greater sensitivity on white areas. These resultsprovide evidence that leaf structure may play an important rolein determining the magnitude of stomatal density and index responsesto CO₂ concentrations.Copyright 1995, 1999 Academic Press Leaf structure, photosynthesis, stomatal conductance, CO₂, stomatal density, stomatal index     

Stomatal responses to a range of variables in two tropical tree species grown with CO2 enrichment

Seedlings of Maranthes corymbosa (Blume) and Eucalyptus tetrodonta(F. Muell) were grown with or without CO₂ enrichment (700µmolCO₂ mol^–1 The response of stomatal conductance (g₂) toleaf drying, exogenous absclslc acid and calcium ions was investigatedin M. corymbosa. Reciprocal transfer experiments were also conductedwhereby plants were grown in one treatment and then transferredto the other before g, was measured. Stomatal conductance in M. corymbosa was more sensitive (a greaterpercentage decline in g₂ per unit percentage decline in leaffresh weight) to leaf water status under conditions of CO₂ enrichmentcompared to ambient conditions. However, the rate of reductionof g₂ in response to exogenous abscisic acid was not influencedby CO₂ treatment. In contrast, the rate of reduction of g₂,in response to exogenous CaCl₂ was decreased under conditionsof CO₂ enrichment. Reciprocal transfer experiments showed that expo sure to CO₂enrichment results in a short-term, reversible decline in g₂,as a result of decreased stomatal aperture and a long-term,irreversible decline in g₂ as a result of a decreased stomataldensity. Seedlings of E. tetrodonta were used to investigate the responseof g₂ to light flux density, leaf-to-air vapour pressure difference(LAVPD), leaf internal CO₂ concentration (C₁ and temperature.Reciprocal transfer experiments were also conducted. CO₂ enrichmentdid not influence the pattern or sensitivity of response ofg to LAVPD and C in E. tetrodonta. In contrast, the slope ofthe response of g₂, to temperature decreased for trees grownunder elevated [CO₂]_a conditions and the equilibrium g₂ attainedat saturating light was also decreased for plants grown underelevated [CO_2a. conditions. Key words: Stomata, elevated CO₂, tropical trees     

28种园林植物对大气CO2浓度增加的生理生态反应

通过对28种园林植物在不同CO2浓度水平下的气体交换参数的观测,分析了净光合速率、气孔导度、蒸腾速率和水分利用效率等生理生态指标的变化趋势与规律.结果表明,所测植物净光合速率和水分利用效率随CO2浓度升高而线性增加,但不同植物种类对高CO2浓度的反应存在较大差异.气孔导度和蒸腾速率与CO2浓度呈线性负相关关系.当CO2浓度倍增(350～700 μmol·mol-1)时,28种园林植物净光合速率平均提高31.2%,气孔导度降低16.5%,蒸腾速率下降11.7%,而水分利用效率则提高了49.2%.不同光合途径的植物净光合速率和水分利用效率受CO2浓度增加的影响程度为C3植物较大,C4植物较小, CAM植物介于两者之间.对不同生活型植物而言,影响程度则为草本C3植物较大,乔木C3植物较小,灌木C3植物居于两者之间.     

Interactions between C3 and C4 salt marsh plant species during four years of exposure to elevated atmospheric CO2

Elevated atmospheric CO2 is known to stimulate photosynthesis and growth of plants with the C₃ pathway but less of plants with the C₄ pathway. An increase in the CO₂ concentration can therefore be expected to change the competitive interactions between C₃ and C₄ species. The effect of long term exposure to elevated CO₂ (ambient CO₂ concentration +340 µmol CO₂ mol^-1) on a salt marsh vegetation with both C₃ and C₄ species was investigated. Elevated CO₂ increased the biomass of the C₃ sedgeScirpus olneyi growing in a pure stand, while the biomass of the C₄ grassSpartina patens in a monospecific community was not affected. In the mixed C₃/C₄ community the C₃ sedge showed a very large relative increase in biomass in elevated CO₂ while the biomass of the C₄ species declined.The C₄ grassSpartina patens dominated the higher areas of the salt marsh, while the C₃ sedgeScirpus olneyi was most abundant at the lower elevations, and the mixed community occupied intermediate elevations.Scirpus growth may have been restricted by drought and salt stress at the higher elevations, whileSpartina growth at the lower elevations may be affected by the higher frequency of flooding. Elevated CO₂ may affect the species distribution in the salt marsh if it allowsScirpus to grow at higher elevations where it in turn may affect the growth ofSpartina.     

Photosynthetic responses to CO2 enrichment of four hardwood species in a forest understory

We compared the CO₂- and light-dependence of photosynthesis of four tree species (Acer rubrum, Carya glabra, Cercis canadensis, Liquidambar styraciflua) growing in the understory of a loblolly pine plantation under ambient or ambient plus 200 μl l^–1 CO₂. Naturally-established saplings were fumigated with a free-air CO₂ enrichment system. Light-saturated photosynthetic rates were 159–190% greater for Ce. canadensis saplings grown and measured under elevated CO₂. This species had the greatest CO₂ stimulation of photosynthesis. Photosynthetic rates were only 59% greater for A. rubrum saplings under CO₂ enrichment and Ca. glabra and L. styraciflua had intermediate responses. Elevated CO₂ stimulated light-saturated photosynthesis more than the apparent quantum yield. The maximum rate of carboxylation of ribulose-1,5-bisphosphate carboxylase, estimated from gas-exchange measurements, was not consistently affected by growth in elevated CO₂. However, the maximum electron transport rate estimated from gas- exchange measurements and from chlorophyll fluorescence, when averaged across species and dates, was approximately 10% higher for saplings in elevated CO₂. The proportionately greater stimulation of light-saturated photosynthesis than the apparent quantum yield and elevated rates of maximum electron transport suggests that saplings growing under elevated CO₂ make more efficient use of sunflecks. The stimulation of light-saturated photosynthesis by CO₂ did not appear to correlate with shade-tolerance ranking of the individual species. However, the species with the greatest enhancement of photosynthesis, Ce. canadensis and L. styraciflua, also invested the greatest proportion of soluble protein in Rubisco. Environmental and endogenous factors affecting N partitioning may partially explain interspecific variation in the photosynthetic response to elevated CO₂. Received: 16 February 1999 / Accepted: 30 August 1999     

Stomatal versus biochemical limitations to dynamic photosynthetic performance in four tropical rainforest shrub species

Photosynthetic performance under dynamic light regimes was assessed in four different species of tropical shrubs from the family Rubiaceae via field gas exchange measurements conducted on Barro Colorado Island, Panamá. Rates of photosynthetic induction and induction loss were assessed throughout the day in both the wet and dry seasons in order to determine the relative roles of stomata and biochemistry in limiting photosynthetic performance under transient light conditions. A high degree of coordination was observed between stomatal conductance and biochemical capacity for CO₂ assimilation during induction. Rates of biochemical and overall photosynthetic induction sharply decreased when initial stomatal conductance fell below a narrow range of critical values. Time of day or season did not affect rates of biochemical deactivation upon shading, but did influence stomatal closure, which often exerted a significant influence over induction loss in the darkness. In measurements of total assimilation due to a 60-s light pulse, both biochemical activity and stomatal conductance were linearly related to total CO₂ uptake. Only during the mornings of the wet season was stomatal conductance consistently high enough to be non-limiting to dynamic photosynthetic performance. At all other times, stomatal behavior exercised significant influence over induction times, photosynthetic induction loss, and total CO₂ uptake from 60-s light pulses. Received: 17 March 1999 / Accepted: 26 October 1999     

The Responses of Stomatal Density to CO2 Partial Pressure

Experiments on a range of species of tree, shrub and herb haveshown that stomatal density and stomatal index increase as thepartial pressure of CO₂ decreases over the range from the currentlevel of 34 Pa to 22.5 Pa. Stomatal density responds to thereduced 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 70Pa stomatal density decreases slightly, with a response to unitchange in CO₂ which is about 10% of that below 34 Pa. Measurements of gas exchange on leaves which had developed indifferent CO₂ partial pressures, but at low saturation vapourpressure deficits in the range of 0.7 to 0.9 kPa, indicatedlower photosynthetic rates but higher stomatal conductancesat reduced CO₂ partial pressures. Experiments on populations of Nardus stricta originating fromaltitudes of 366 m and 810 m in Scotland, indicated geneticdifferences in the responses of stomatal density to CO₂ in pressuressimulating altitudes of sea level and 2 000 m. Plants from thehigher altitude showed greater declines in stomatal densitywhen the CO₂ partial pressure was increased. Key words: Stomata, CO₂, gas exchange, altitude, atmospheric pressure     

Influence of CO2 on Stomatal Numbers

From nine different plant species grown at 1500 cm³ m^-3 CO₂ five responded with a significant increase in stomatal numbers per mm² as compared with plants grown under normal air conditions. Within a collection of twelve french bean cultivars remarkable cultivar differences with regard to the CO₂ enhancement effect on stomatal numbers was found.     

Stomatal responses to light and CO2 in greening wheat leaves

The development of two types of stomatal transpiration, oneinduced by light (light-induced stomatal transpiration) andthe other induced by CO₂-free air in the dark (CO₂-sensitivestomatal transpiration), in greening leaves of wheat (Triticumaestivum L.) was studied in respect to the development of CO₂uptake and chlorophyll formation. Light-induced stomatal transpirationwas not observed at all in etiolated leaves and was generatedafter 3 hr of illumination for greening, when the activity ofCO₂ uptake was generated. CO₂-sensitive stomatal transpirationwas low in etiolated leaves and started to increase at the sametime during greening as the start of CO₂ uptake. The activitiesof both light-induced and CO₂-sensitive stomatal transpirationincreased as the activity of CO₂ uptake and the chlorophyllcontent increased. Pre-illumination of etiolated leaves for1 min followed by 4 hr of dark incubation eliminated the lagfor the development of the two types of stomatal transpirationand CO₂ uptake. (Received September 4, 1978; )     

Stomatal frequency responses in hardwood-swamp vegetation from Florida during a 60-year continuous CO2 increase

In a stomatal frequency analysis of leaf remains of Quercus nigra, Acer rubrum, Myrica cerifera, Ilex cassine, and Osmunda regalis that were preserved in precisely dated peat deposits of north-central Florida, the stomatal index decreased as a response to an atmospheric CO(2) increase from 310 ppmv to 370 ppmv over the past 60 years. The observations indicate that CO(2) responsiveness may occur in different canopy levels of hardwood-swamp vegetation. Apart from common woody plants, long-lived ferns of the undergrowth appear to be affected by CO(2) changes. Response rates are most pronounced in M. cerifera, I. cassine, and O. regalis. The potential of these species for quantifying past atmospheric CO(2) levels is assessed by a combined analysis of the well-dated buried leaf record and herbarium material collected during the past century. Leaf remains of the widely occurring species M. cerifera and I. cassine are concluded to be highly suitable for CO(2) reconstructions, by which the application range of the stomatal frequency proxy is extended into the warm-temperate to subtropical realm of North America.     

Drawing the future: Stomatal response to CO2 levels

Gas exchange between the plant and the atmosphere is regulated by controlling both the stomatal density and the aperture of the stomatal pore. Environmental factors such as light, the level of atmospheric CO₂ and hormones regulate stomatal development and/or function. Because atmospheric CO₂ levels have been rising since the Industrial Revolution, and it is predicted that they will continue doing so in the future, an understanding of the CO₂ signalling mechanisms in the stomatal responses will help to know how plants were in the past and will allow predicting how they will respond to climate change in the near future. This article covers the recent knowledge of the CO₂ signalling mechanisms that regulate both stomatal function and development.Key words: Arabidopsis, CO₂, development, epidermis, gas exchange, leaf, patterning, stoma     

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

Background and Aims

The inverse relationship between stomatal density (SD: number of stomata per mm² leaf area) and atmospheric concentration of CO₂ ([CO₂]) permits the use of plants as proxies of palaeo-atmospheric CO₂. Many stomatal reconstructions of palaeo-[CO₂] are based upon multiple fossil species. However, it is unclear how plants respond to [CO₂] across genus, family or ecotype in terms of SD or stomatal index (SI: ratio of stomata to epidermal cells). This study analysed the stomatal numbers of conifers from the ancient family Cupressaceae, in order to examine the nature of the SI–[CO₂] relationship, and potential implications for stomatal reconstructions of palaeo-[CO₂].

Methods

Stomatal frequency measurements were taken from historical herbarium specimens of Athrotaxis cupressoides, Tetraclinis articulata and four Callitris species, and live A. cupressoides grown under CO₂-enrichment (370, 470, 570 and 670 p.p.m. CO₂).

Key Results

T. articulata, C. columnaris and C. rhomboidea displayed significant reductions in SI with rising [CO₂]; by contrast, A. cupressoides, C. preissii and C. oblonga show no response in SI. However, A. cupressoides does reduce SI to increases in [CO₂] above current ambient (approx. 380 p.p.m. CO₂). This dataset suggests that a shared consistent SI–[CO₂] relationship is not apparent across the genus Callitris.

Conclusions

The present findings suggest that it is not possible to generalize how conifer species respond to fluctuations in [CO₂] based upon taxonomic relatedness or habitat. This apparent lack of a consistent response, in conjunction with high variability in SI, indicates that reconstructions of absolute palaeo-[CO₂] based at the genus level, or upon multiple species for discrete intervals of time are not as reliable as those based on a single or multiple temporally overlapping species.