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Ecology |
2Laboratory of Palaeobotany and Palynology, Utrecht University, 3584 CD Utrecht, Netherlands; 3Department of Geology, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, Illinois 60605 USA; 4Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN UK; 5Department of Geography, University of Leicester, Leicester LE1 7RH UK
Received for publication July 30, 2002. Accepted for publication November 12, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: CO2 • conifers • leaf morphology • North America • quantification methods • stomata • stomatal density
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Woodward and Kelly, 1995
; Royer, 2001
). This inverse relation between stomatal frequency and atmospheric CO2 is even more apparent under lower-than-present experimental CO2 levels (Woodward, 1987
; Woodward and Bazzaz, 1988
; Malone et al., 1993
; Royer, 2001
). A genetic basis for the response is provided by the identification of a CO2-sensitive gene in Arabidopsis thaliana that is involved in the control of stomatal development (Gray et al., 2000
). The relation between stomatal frequency and atmospheric CO2 concentration (mixing ratio; measured as parts per million by volume [ppmV]) is confirmed by studies of leaves that were grown under the lower CO2 levels of the past 100 yr. Such leaves can be obtained from herbarium collections or subfossil leaf assemblages. The main advantage of historical leaf material over experimental material is that the stomatal frequency responses to CO2 have occurred under natural conditions. Effects of experimental single-step CO2-enrichment (typically CO2-doubling) on seedlings may not be representative of long-term responses to incremental increases of 1 to 2 ppmV CO2 per year or per growing season.
Notably leaves of woody angiosperm taxa show a negative correlation between mean stomatal frequency and the historical CO2 rise from 280 to 360 ppmV (Woodward, 1987
; Peñuelas and Matamala, 1990
; Paoletti and Gellini, 1993
; Kürschner et al., 1996
; Wagner et al., 1996
; Wagner, 1998
). Modelled response curves for species of Betula and Quercus predict different response limits to a CO2 increase (
400 and 340 ppmV, respectively), indicating that nonlinear stomatal frequency responses vary from one tree species to another (Kürschner et al., 1997
). The models also suggest that the maximum effect of the current CO2 increase on stomatal frequency has already been reached, thereby explaining the common lack of stomatal frequency responses in CO2-doubling experiments.
Conifers and broad-leaved angiosperms have basic differences in stomatal formation and leaf development (Esau, 1977
). In angiosperms, stomata and epidermal cells are initiated at multiple points on the developing leaf surface, resulting in a relatively random distribution of stomata on the entire leaf surface. Epidermal cells and stomata in conifer needles are all initiated at the base of the needle, developing henceforth in longitudinal files during needle growth (Croxdale, 2000
). Conifers have a less-pronounced decrease in stomatal conductance than angiosperms in response to long-term, elevated CO2 exposure (Saxe et al., 1998
; Medlyn et al., 2001
). Because stomatal conductance is in part determined by the number of stomata on the leaf surface (Jones, 1992
), in theory different responses could be related to differences in the adjustment of stomatal frequency to CO2 levels.
To date, only six experiments have been performed to test whether the typical arrangement of stomata in conifer needles affects stomatal frequency responses to atmospheric CO2 (Royer, 2001
). A frequency decrease in Pinus sylvestris under elevated CO2 (Beerling, 1997
; Lin et al., 2001
) suggests that conifers also may have the capacity to adjust their stomatal numbers. However, stomatal frequency in other species (Pinus pinaster, P. banksiana, P. palustris, Pseudotsuga menziesii, and Picea abies) is not reduced at elevated CO2 levels (Stewart and Hoddinott, 1993
; Guehl et al., 1994
; Dixon et al., 1995
; Pritchard et al., 1998
; Apple et al., 2000
). This lack of reduction could indicate that in many conifer species, stomatal frequency is not very sensitive to CO2 changes. On the other hand, the controlled-environment experiments may have been performed under CO2 levels that are well above the response limit to a CO2 increase.
In addition to experimental studies, the CO2 responsiveness of two conifer species has been confirmed by analyses of fossil and herbarium materials. Van de Water et al. (1994)
have reported elevated stomatal frequencies in fossil needles of Pinus flexilis corresponding to a CO2 range from 180 to 290 ppmV. Recently, in an herbarium study on needles of Metasequoia glyptostroboides, stomatal frequency decreased linearly over a CO2 range from 310 to 340 ppmV (Royer et al., 2001
). Additional experiments on Metasequoia under CO2 concentrations of 430 and 790 ppmV showed a nonlinear response, similar to the response curves of angiosperm species, levelling off at about 500 ppmV. Obtaining these response curves is hampered by the fact that most experiments involve a single-step doubling of CO2. To compare the CO2 response curves of conifers to those of angiosperms, the stomatal frequency must be measured over a gradual increase in CO2.
Historical data sets enable the construction of accurate response curves that can be used as training sets for the quantification of past atmospheric CO2 levels on the basis of stomatal frequency analysis of fossil leaves (Van der Burgh et al., 1993
; Beerling et al., 1995
; Kürschner et al., 1996
; Rundgren and Beerling, 1999
; Wagner et al., 1999
; McElwain et al., 2002
). Considering the dominance of conifers in temperate and boreal forest ecosystems, the ability to use fossil conifer needles for quantifying past CO2 levels would greatly extend the spatial and temporal coverage of such reconstructions. In North America, well-preserved needles of Tsuga heterophylla, Picea glauca, P. mariana, and Larix laricina are often present in Quaternary lake and peat deposits (Dunwiddie, 1986
; Cwynar, 1987
; Mayle and Cwynar, 1995
).
To assess the CO2 responsiveness of conifer needles, as well as their potential as biosensors of paleo-atmospheric CO2 fluctuations, the present study focuses upon the stomatal frequency response of these species to a range of historical CO2 values (290–370 ppmV). Customized counting strategies are introduced to account for the typical stomatal patterning in conifers needles.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Some of the needles of Tsuga heterophylla used in the study were obtained from the collection of the National Herbarium of the Netherlands, complemented with needles from living trees collected in the field in 1998 and 2000. The material originates from 13 localities in the Northwest Pacific area of the USA and Canada; 8–11 needles from each locality were processed (Fig. 1). Additionally, assemblages of subfossil Tsuga heterophylla needles were derived from an 8-cm-long peat core taken at the margin of Jay Bath, a pond in Mount Rainier National Park (Washington, USA; 46°46' N, 121°46' W). Eleven of the annual layers in this core, spanning a period from 1980 to 1998, yielded 3–5 Tsuga heterophylla needles each. A total of 160 Tsuga heterophylla needles from herbaria, living trees, and the peat core were analyzed for stomatal frequency.
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Methods
The needles of Tsuga heterophylla were bleached with a 4% natriumhypochloride solution to remove the mesophyll. The remaining cuticle was then stained with safranin and mounted in glycerin jelly on a microscopic slide. Computer-aided measuring of epidermal cell parameters on needle cuticles of Tsuga heterophylla was performed on a Leica Quantimet 500C/500+ Image Analysis system (Wetzlar, Germany). Stomata on Picea and Larix needles were counted directly from whole unprepared needles using a Leica epifluorescence microscope. Regression analysis and Student's t test were performed using SPSS 8.0 for Windows statistical software (Chicago, Illinois, USA).
The presence of tephra from the 1980 eruption of Mt. St. Helens (Mullineaux, 1974
, 1996
) enabled a precise age assessment of the annual layers apparent in the peat core from Jay Bath.
The atmospheric CO2 mixing ratios for the past 100 yr that were used in the response curves were derived from instrumental measurements at Mauna Loa since 1957 (Keeling and Whorf, 2002
) and shallow Antarctic ice cores (Etheridge et al., 1996
; Indermühle et al., 1999
). Records of temperature and precipitation at Mount Rainier were obtained from the IRI/LDEO Climate Data Library (website: http://ingrid.ldeo.columbia.edu).
Expression of stomatal frequency
Stomatal frequency is conventionally expressed as stomatal density (the number of stomata per unit leaf area) or as stomatal index (the proportion of stomata expressed as a percentage of total epidermal cells). Stomatal index is generally favored because it accounts for the influence of lateral cell expansion related to water availability on stomatal density (Salisbury, 1927
; Kürschner et al., 1996
; Kürschner, 1997
).
The stomata on conifer needles are arranged in rows, occurring in either single files (Larix laricina) or grouped in bands (Tsuga heterophylla, Picea glauca/mariana; Fig. 2). Therefore, in contrast to broad-leaved species, stomatal placement and occurrence on conifer needles is not well characterized through the measurement of either stomatal density or index in small counting fields.
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The lower surface of the hypostomatal Tsuga heterophylla needles displays two broad bands of stomatal rows on each side of the central vein (Fig. 2), while four stomatal bands are present on the surface of the four-sided amphistomatal Picea glauca/mariana needles. In this way, the leaf surface is divided into stomate-free (midvein, leaf margins) and stomatal regions (the bands). Consequently, the stomatal frequency on the needles of these species not only varies in terms of stomatal density/index within the bands, but also by the extent of the stomatal regions on the needle surface. Thus, for Tsuga heterophylla and Picea glauca/mariana stomatal index and density within the bands were measured, as well as the width of the bands and the total number of stomata per millimeter of needle length.
To account for the varied stomatal patterning in conifer needles, the following customized stomatal quantification methods were applied in this study.7
Stomatal density (SD) was measured as the number of stomata per square millimeter of leaf area. On Tsuga heterophylla needles, SD was measured in 10 counting fields (0.057 mm2) within the stomatal bands at a magnification of 500x. For Picea glauca/mariana needles, SD was measured on the abaxial surface in 2–10 counting fields spanning the entire width of a band along the length of a calibrated 0.800-mm scale bar at a magnification of 200x.
Stomatal index (SI) was measured as (the number of stomata divided by the number of stomata plus epidermal cells) x100. On Tsuga heterophylla needles, SI was calculated based on stomatal and epidermal cell counts in 12 counting fields spanning the width of a band along a 0.400-mm needle length. On Picea glauca/mariana needles, SI was calculated based on stomatal and epidermal cell counts in 2–10 counting fields spanning the width of a band along the length of a calibrated 0.800-mm scale bar.
Stomatal number per Length (SNL) was measured as (the number of abaxial stomata plus the number of adaxial stomata) divided by needle length in millimeters. On Larix laricina needles, SNL was measured in 2–10 counting fields along the length of a calibrated 0.800-mm scale bar at a magnification of 200x.
Stomatal rows (SR) was measured as the number of stomatal rows in both stomatal bands. This method quantifies the extent of the stomatal regions on the Tsuga and Picea needles. Band width is highly dependent of the number of rows in a band, as measured in 35 perfectly preserved modern Tsuga heterophylla needles (n = 700; Pearson correlation, 0.953). Band width is expressed as number of rows rather than absolute width (in millimeters) because the former is easier to measure (especially in less well-preserved [fossil] needles). For Tsuga heterophylla, the number of rows in both bands was counted along 10 transects perpendicular to the needle axis and restricted to the middle third part of the needle because the number of rows decreases strongly at the tip and the base of the needles (Fig. 2). For the amphistomatal Picea glauca/mariana, mean number of rows per needle (on both sides) was determined.
Stomatal density per length (SDL) was determined using the equation SDL = SD x SR. Stomatal density per length combines stomatal density within the bands and the width of the bands, providing a measure of the total number of stomata per millimeter of needle length in Tsuga heterophylla and Picea glauca/mariana needles. Because SR is the number of rows instead of the true band width (in millimeters), SDL represents a general indication of the number of stomata per millimeters needle length, capable of reflecting changes in stomatal frequency. The expression of band width in number of rows rather than absolute distance also explains the apparent discrepancy of expressing SDL per square millimeters instead of per millimeter.
True stomatal density per length (TSDL) was determined using the equation TSDL = SD x band width (in millimeters). The number of stomata per millimeter of needle length (TSDL) can be approximated more accurately when the band width is expressed in millimeters instead of number of rows. The TSDL was calculated only for Tsuga heterophylla, using the linear relation between SR and band width (in millimeters) as measured in 35 perfectly preserved modern Tsuga heterophylla needles (n = 700; Pearson correlation, 0.953).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Conifer leaves develop linearly from a single growth center at the needle base, similar to monocots, instead of from multiple point sources on the leaf as in broad-leaved angiosperms (Croxdale, 2000
). Epidermal cells appear in longitudinal files, with the cells at the tip of the leaf maturing first. Stomatal formation in conifers takes place during a late stage of leaf growth. Guard cells of Pseudotsuga menziesii, for example, do not become apparent until the needle has reached two-thirds of its final size (Owens, 1968
). When the stomatal precursor cells form in specific rows, the epidermal cells in the adjacent files of cells divide asymmetrically to produce subsidiary cells lying directly next to the stomatal precursor cells and epidermal cells in the adjacent cell file (Fig. 6; Croxdale et al., 1992
; Larkin et al., 1997
). In many conifer species and monocots, the latter epidermal cells can continue to divide a specific number of times creating a species-specific fixed number of epidermal cells in the "stomatal-epidermal complex" (Tomlinson, 1974
). These complexes can contain between four and 12 epidermal cells each, depending on the species (Florin, 1931
). When stomata are densely packed, as in Tsuga and Picea, nearly all epidermal cells encountered in the stomatal bands belong to the stomatal-epidermal complexes, except for a few very elongated pavement cells in rows of epidermal cells (Fig. 7). In these cases of densely packed stomata, the number of epidermal cells in the bands will mainly depend on the number of stomata present, keeping SI constant. The SD reflects stomatal initiation rate much better than the SI. Because epidermal cells from the stomatal complexes should be excluded from the ratio, the application of SI as an expression of stomatal frequency in conifers should be restricted to species with a significant number of pavement epidermal cells. This phenomenon may also explain in part why little or no stomatal response has been observed in grasses growing in elevated CO2. The number of subsidiary cells can be affected by CO2 levels (Boetsch et al., 1996
), but pavement and stomatal complex epidermal cells in mature conifer leaves cannot always be easily distinguished (Florin, 1931
). Therefore, the size of the stomatal complexes and the number of pavement epidermal cells in a conifer species should be taken into account before using a SD- or SI-based counting strategy.
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Concerning conifer taxa with single stomatal rows (such as Pinus and Larix), care should also be taken to capture the variability in the number of rows as well as the variability in the number of stomata per row. This can be achieved by measuring SNL, the total (abaxial and adaxial) number of stomata per millimeter of needle length. If small counting fields are used (less than half of the needle width) for conventional SD measurements, minor variations in the number of rows will not be reflected, and stomatal row numbers should be included in the quantification of stomatal frequency.
Validation of the stomatal frequency response to CO2
In the present study SD-based counting strategies are applied instead of SI-based methods. The SD depends not only on stomatal initiation rate, but also on lateral cell expansion after stomatal formation, which can be strongly influenced by environmental factors other than atmospheric CO2. To determine if the observed changes in stomatal frequency in the conifers can be ascribed to the rise in CO2 over the last century, the potential influence of environmental and biological variations (geography, altitude, light regime, humidity, temperature, and ontogeny) on stomatal frequency has to be evaluated.
Geography
Because the conifer needles in this study were collected in varying geographical regions, interpretation of the observed responses could be complicated by differences in climate at the source localities and genotypic dissimilarities between different populations. Contrasting sampling strategies for Tsuga heterophylla vs. Picea glauca/mariana and Larix laricina were used to deal with the potential influence of variation in climate and populations on the stomatal frequency.
All Tsuga heterophylla needles (from living trees, herbarium sheets, and subfossil peat) were collected in the Northwest Pacific region of the USA/Canada and have thus grown under similar temperate conditions with high precipitation, minimizing the potential influence of large climatic variations. The modern samples (Fig. 3: 363 and 367 ppmV) were collected from living trees at several sites in British Columbia and Washington. The considerable variation in stomatal frequency in these modern samples may reflect intrinsic variability between trees, phenotypical responses to micro-climatic differences between these sites, and differences in local CO2 mixing ratios present at forested sites (Tarnawski et al., 1994
). Despite the variation in stomatal frequency, the TSDL (the most sensitive quantification method) of the modern samples is consistently low and the decreasing trend in mean stomatal frequency in the data set is substantial and significant.
Subfossil and modern needles, which were derived from a single population of trees around Jay Bath over the last 20 yr, are indicated by black diamonds in Fig. 3D. The TSDL changes in this restricted data set (within a single population) do not differ significantly from the TSDL decrease observed in the total data set, which includes data points from other localities (and populations). Thus, there are no indications that the observed stomatal frequency changes in Tsuga heterophylla reflect variations in stomatal frequency between different populations.
A reverse sampling strategy was employed for Picea glauca/mariana and Larix laricina. Herbarium material from these species was chosen from a wide range of localities in northern USA and Canada, within the species' natural climatic ranges and tolerances. Herbarium leaves of cultivated trees from Scotland, North America, and England were also included in the calibration data sets because no significant differences in stomatal frequencies were observed between trees growing in cultivation and in nature under the same CO2 levels. By maximizing variation in climate and populations in the data set, the potential effect of biological and environmental factors other than CO2 on stomatal frequency of Picea and Larix is expressed within the statistical confidence intervals of the regression data set. Because the decrease in stomatal frequency appears both within a single population and in a data pool of maximized environmental variation, the stomatal response to CO2 of the studied conifer species is unlikely to be an artefact caused by differences in populations and climate associated with the geographical variation in the data sets.
Altitude
Although the CO2 mixing ratio in air remains constant over altitudinal gradients, the CO2 partial pressure (as measured in pascals) is lower at higher elevation because of the decrease in air pressure. Stomatal frequency responds to altitude-controlled changes in CO2 partial pressure when CO2 mixing ratio is unaltered (Woodward and Bazzaz, 1988
). To check whether the observed stomatal frequency decrease in Tsuga heterophylla could be related to altitudinal differences in the data set (sea level to 1600 m), an alternative response curve was plotted using only needles grown at altitudes in the range of Jay Bath (1200–1600 m; Fig. 8). The stomatal frequency response in Tsuga heterophylla needles from this restricted altitudinal range is not significantly different from the response in the original data set with needles from a broader altitudinal range (Fig. 3D). For Picea glauca, P. mariana, and Larix laricina, leaf material from herbarium sheets collected from high elevations was not included in the data sets to avoid the effects of decreased CO2 partial pressure with increasing elevation on stomatal frequency. Thus, the observed stomatal frequency response in the conifer species is not significantly affected by the altitudinal variation in the data set.
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; Lichtenthaler, 1985
; Kürschner, 1997
), additional stomatal frequencies were measured for Tsuga heterophylla needles that were grown under sunny and shady light regimes at the botanical gardens in Utrecht (Netherlands). No significant difference in either SD, SR, or TSDL could be detected in the needles grown under contrasting light regimes (shade: 177 ± 36 stomata/mm, sun: 174 ± 18 stomata/mm; P = 0.883 for TSDL; L. L. R. Kouwenberg, unpublished data). Hence, the observed relation between CO2 and TSDL in Tsuga heterophylla is not significantly affected by the varying light intensity under which the herbarium and fossil needles may have developed. The observed TSDL values of these needles are highly comparable to the modern material from the Northwest Pacific region of North America.
Water availability
Water availability determines cell expansion and thus stomatal density on leaf surfaces (Salisbury, 1927
; Tichá, 1982
). Therefore it must be considered whether the observed SD decrease in the data set could be a result of local changes in soil water availability during the last century. Annual and spring precipitation records measured at Longmire (Mount Rainier) from 1930 to 2002 were compared to the stomatal frequency records of Tsuga heterophylla (Fig. 9A). These records do not show any long-term unidirectional increase in precipitation that might have triggered the observed reduction in stomatal frequency.
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). Thus, monthly temperature records from Longmire were also compared with the stomatal frequency records of Tsuga heterophylla (Fig. 9B). Both spring and annual temperatures increased 0.8°C between 1915 and 1940 but showed no further long-term unidirectional change. Thus, differences in growing temperature are highly unlikely to have influenced the decrease in stomatal frequency.
Ontogeny
Marked variations in SD are reported for angiosperm leaves during leaf ontogeny (Tichá, 1982
). Considering the specific leaf development and stomatal initiation in conifers, ontogenetical differences in stomatal frequency on conifer needles could be expected to be less pronounced. Measurements of SD, SR, and TSDL on developing Tsuga heterophylla needles from the same branch were indeed not significantly different in these stomatal frequency parameters for young and fully grown needles (mean needle length of 7.2 and 12.0 mm, respectively; L. L. R. Kouwenberg, unpublished data).
Stomatal frequency response rates
The four conifer species analyzed in this study show a significant reduction in stomatal frequency as a response to a CO2 rise of 80 ppmV over the last century. The response rates, a 4.49% decrease in TSDL per 10 ppmV of CO2 increase for Tsuga heterophylla and a 7.34% and 8.09% decrease in SDL for Picea mariana/glauca and Larix laricina, respectively, are comparable with the SI response rates for angiosperm tree taxa commonly used for CO2 analysis of fossil leaves (Betula: –5.47% of the SI per 10 ppmV of CO2, Quercus –3.82%). Thus, over a CO2 range between 290 and 370 ppmV, stomatal frequency adjustment in conifers can occur at a similar rate as in woody angiosperms. Furthermore, earlier suggestions that the response of conifers in general would level off at CO2 values of 280 ppmV (Van de Water et al., 1994
) are refuted by the observation that both Tsuga heterophylla and Picea glauca/mariana have not reached their response limit yet at the current CO2 level of 370 ppmV. Thus, similar to angiosperms, conifers (Pinus, Metasequoia, Tsuga, Picea, Larix) may have species-specific response ranges. Several conifer species still respond to increases in CO2 above the response limits for angiosperm species used for stomatal frequency analysis, making them very suitable for the reconstruction of paleo-atmospheric CO2 concentrations well above present levels (Royer et al., 2001
).
Conclusions
The capability of conifers to adjust their stomatal frequency to changes in atmospheric CO2 mixing ratios has now been confirmed in four more conifer species. Tsuga heterophylla, Picea glauca, P. mariana, and Larix laricina show a strong reduction in stomatal frequency in accordance with a change in historical CO2 levels from 290 to 370 ppmV. Because of their sensitive response over a broad range of CO2 levels, combined with a high preservation capacity, fossil needles of the studied conifer species show great potential for paleo-atmospheric CO2 reconstructions. Considering the dominance of conifers in temperate and boreal forest ecosystems (in both the Northern and Southern Hemisphere), the spatial and temporal coverage of such reconstructions may thus be markedly extended. This is corroborated already by results of ongoing research in the Northwest Pacific region of the USA (L. L. R. Kouwenberg et al., unpublished manuscript and Atlantic Canada (McElwain et al., 2002
). Furthermore, the observation that all four conifer species have not yet reached their response limits to CO2 suggest that paleo-CO2 estimates derived from conifers rather than angiosperms may be preferable during those times in the Earth's history when greenhouse gas concentrations were much higher than present (such as during the Cretaceous).
The specific stomatal patterning on conifer needles has precluded the application of stomatal index measurements as a CO2-sensitive expression of stomatal frequency. New quantification methods, based on the number of stomata per millimeter of needle length, are proposed as the most accurate measure of stomatal frequency in conifer species. In general, stomatal quantification methods should be tailored to specific leaf development and subsequent stomatal patterning of the species studied.
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FOOTNOTES |
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6 Author for reprint requests (L.L.R.Kouwenberg{at}bio.uu.nl
)
7 Methods have been developed independently in Utrecht and Sheffield.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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