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(American Journal of Botany. 2005;92:690-695.)
© 2005 Botanical Society of America, Inc.

Ecology

Stomatal frequency responses in hardwood-swamp vegetation from Florida during a 60-year continuous CO2 increase1

Friederike Wagner2,4, David L. Dilcher3 and Henk Visscher2

2Palaeoecology, Laboratory of Palaeobotany and Palynology, Utrecht University, 3584 CD Utrecht, The Netherlands; 3Florida Museum of Natural History, Gainesville, Florida 32611 USA

Received for publication March 18, 2004. ABSTRACT

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 CO2 increase from 310 ppmv to 370 ppmv over the past 60 years. The observations indicate that CO2 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 CO2 changes. Response rates are most pronounced in M. cerifera, I. cassine, and O. regalis. The potential of these species for quantifying past atmospheric CO2 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 CO2 reconstructions, by which the application range of the stomatal frequency proxy is extended into the warm-temperate to subtropical realm of North America.

Key Words: atmospheric CO2 • Florida • peat deposits • stomatal index • subfossil leaves

The quantification of adjustment in stomatal frequency in C3 plants to historical man-induced atmospheric increase in CO2 enables the reconstruction of past CO2 levels through stomatal frequency analysis of leaf remains commonly buried in peat and lake deposits (Wagner et al., 1996 ; Poole and Kürschner, 1999 ; Kürschner et al., 2001 ; Royer, 2001 ). Validation and application of this botanical proxy has been successfully performed with a variety of common broadleaved tree and shrub species, as well as some conifer species. The majority of the taxa currently used for CO2 reconstructions originate from the mid to high latitudes of Europe and North America (Rundgren and Beerling, 1999 ; Wagner et al., 1999 , 2002 , 2004 ; McElwain et al., 2002 ; Kouwenberg et al., 2003 ; Rundgren and Björck, 2003 ).

While the number of species studied from temperate to subarctic environments is increasing, only sparse information is available on the response of plants from the warm-temperate to (sub-) tropical realm (Greenwood et al., 2003 ). Finding suitable genera for atmospheric CO2 reconstructions from such environments would increase the applicability of stomatal frequency analysis in several ways. First of all, the geographical range of data sets would be substantially broadened. Inclusion of leaf material from lower latitudes would eliminate potential uncertainties induced by the high seasonal CO2 fluctuations that characterize higher latitudes (Keeling and Whorf, 2003 ). Moreover, in high-latitude environments the presence or absence of leaves of temperature-sensitive species is controlled by climate fluctuations on a glacial–interglacial scale as well as during smaller climatic deteriorations like the Younger Dryas (McElwain et al., 2002 ). In the relatively stable warm-temperate to subtropical environments, long-term leaf records of individual species can be expected to be much more continuous.

In this study, continuously accumulated leaf material preserved in young peat deposits in a hardwood swamp near Gainesville (north-central Florida, USA) was investigated. A high-resolution 14C chronology of the peat from the site "Alligator Crossing" reveals an age of nearly 60 years for the sequence, which corresponds to about 60 ppmv atmospheric CO2 increase since the 1940s.

Abundant leaf remains in the peat deposits represent a variety of species from both canopy and undergrowth. Multiple species analysis provides the opportunity to assess whether pronounced stomatal frequency responses to increasing CO2 remain restricted to specific components or storeys of the vegetation or if they form a more general pattern in the entire plant community.

Selected species from Alligator Crossing having a pronounced CO2 responsiveness were tested for their applicability in CO2 reconstruction by complementary analysis of regionally collected and precisely dated herbarium specimens covering the CO2 increase of the 20th century. Based on the response rates quantified in the resulting herbarium training sets, CO2 inference models were developed. Their predictive accuracy was finally assessed by applying the models to the fossil stomatal frequency data from Alligator Crossing, which allowed direct comparison of the resulting CO2 estimates with the known historical CO2 concentrations at time of leaf accumulation in this well-dated peat sequence.

MATERIAL AND METHODS

A total of 547 subfossil and herbarium leaf samples were studied for their epidermal properties (Table 1). The species studied included (1) representatives of upper canopy deciduous trees: Quercus nigra (Fagaceae) and Acer rubrum (Aceraceae); (2) middle canopy elements: Myrica cerifera (Myricaceae) and Ilex cassine (Aquifoliaceae); and (3) a typical undergrowth fern: Osmunda regalis (Osmundaceae). The first four species account for more than 50% of the entire woody vegetation at the site studied. Complementary herbarium material was analyzed for M. cerifera, I. cassine, and O. regalis. Herbarium materials are from the University of Florida Herbarium (FLAS) and the Nationaal Herbarium Nederland (NHN, Utrecht University branch) collections and originate from various locations, mainly in Florida.


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  		Table 1. Source and total number of leaves analyzed per species

 
The subfossil leaf material comes from an 80-cm sediment core taken in 1998 at a site, locally known as Alligator Crossing, in a mixed hardwood swamp in Gainesville, Alachua County, north-central Florida (29°39'35'' N, 82°15'14'' W; Fig. 1). The top 40 cm of the core is largely composed of accumulated leaf material, the lowermost part is sandy. The leaf-containing part of the core was sampled at 20 intervals of 2 cm each. The 20 samples were sieved; leaf remains were separated and identified by leaf and cuticle characteristics.



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  		Fig. 1. Location map of site, Alligator Crossing, Gainesville, Florida, USA. Photograph shows the densely vegetated coring site situated in a hardwood swamp

 
For microscopic analysis, leaf pieces of approximately 0.5 x 0.5 cm were bleached in 4% sodium hypochlorite solution for a few minutes up to 12 h. From the bleached samples, the lower cuticles were removed, stained in safranin O, and mounted in glycerin jelly.

Standardized, computer-aided determinations of epidermal parameters were performed on a Leica Quantimet 500C/500+ (Rijswijk, The Netherlands) and an AnalySIS image analysis system (Münster, Germany). On 7–10 stomata-bearing alveoles per leaf sample, epidermal cell density (ED [n/mm2]) and stomatal density (SD [n/mm2]) were measured. From SD and ED, the area-independent stomatal index was calculated as percentage stomatal index, SI = [stomatal density/(stomatal density + epidermal cell density)] x 100 (Salisbury, 1927 ). Historical atmospheric CO2 concentrations used for calibration are annual means as measured on Mauna Loa since 1952 (Keeling and Whorf, 2003 ), supplemented by CO2 measurements from Antarctic ice cores (Siple Station; Neftel et al., 1994 ).

RESULTS

Age assessment
Determination of the age of the peat section is based on five accelerator mass spectrometry (AMS) 14C datings (Table 2) performed on single M. cerifera leaf fragments. 14C data were calibrated using a combined wiggle-match and 14C bomb-puls approach developed for very young peat sections (Donders et al., 2004 ). Additional age constraints are 1998 for the core top and 1978 for sample AC 11, in which the first pine-needle fragments indicate the presence of slash pines (Pinus elliottii) at Alligator Crossing (Table 2). Tree-ring analysis in 2002 of the two oldest pine trees at the site indicated an age of 24 years for both individuals.


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  		Table 2. Age determinations for peat core from Alligator Crossing, north-central Florida

 
The best fit for the age–depth model, including all seven datings, was a second order polynomial function (Fig. 2). Due to compaction and decomposition of the leaf material, the time-span covered per 2-cm sample progressively increased from 2 yr/horizon in the uppermost sample to 5 yr/horizon in the lowermost sample.



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  		Fig. 2. Age-depth model for the 40-cm peat section at Alligator Crossing. Closed circles are the core top and calibrated AMS 14C datings, open circle indicates the age of the pine trees at Alligator Crossing. The y-error bars are the age ranges per 2-cm sample, increasing from 2–5 years due to compaction and decomposition of the leaf material

 
Stomatal frequency
Mean SI values and standard deviations per horizon of the five species studied in the Alligator Crossing peat section are shown in Fig. 3A–D. The data are plotted against measured historical atmospheric CO2 concentrations on the linear primary x-axis, corresponding to the age of the sampled horizons shown on the secondary x-axis. In all species studied, mean SI values decreased over the 60 ppmv CO2 increase covered by the peat record.



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  		Fig. 3. Mean stomatal index (SI) values and standard deviations per horizon of the species studied at Alligator Crossing during the global atmospheric CO2 increase from 308 to 368 ppmv CO2 (primary x-axis). CO2 concentrations are annual means measured at Mauna Loa, Hawaii, USA at time of growth, which is inferred from the age assessment for Alligator Crossing (secondary x-axis)

 
The SI of subfossil Q. nigra samples (Fig. 3A, open diamonds) over the CO2 range from 323 ppmv to 368 ppmv, changed by 1.91% SI from mean maximum (max.) 21.41% SI to mean minimum (min.) 19.50% SI (R2 = 0.48; P = 0.1). The SI of subfossil A. rubrum samples (Fig. 3A, open squares) over the CO2 range from 308 ppmv to 371 ppmv changed by 2.31% SI from mean max. 17.71% SI to mean min. 15.40% SI (R2 = 0.36; P = 0.04). With relatively high mean standard deviations of 1.91% SI in Q. nigra and 2.09% SI in A. rubrum reflecting the intrinsic variability of the species, the total variability is equal or close to the observed range of SI reduction over the CO2 increase during the time period studied.

More pronounced changes over the 60 ppmv CO2 increase are observed for M. cerifera, I. cassine, and O. regalis. In M. cerifera (Fig. 3B), SI decreases from mean 20.48% at 308 ppmv CO2 to mean 16.76% at 368 ppmv CO2 by 3.73% (P = 0.002) with an average standard deviation of the total population of 2.09%. In I. cassine (Fig. 3C), SI decreases by 3.82% SI from mean max. 17.26% at 308 ppmv CO2 to mean min. 13.44% at 362 ppmv CO2 (P < 0.0001) with an average standard deviation of all samples of 1.90% SI. The SI of O. regalis (Fig. 3D) changed by 6.11% from mean 22.56% at 308 ppmv CO2 to 16.45% at 368 (P < 0.0001) with an average standard deviation of 3.15%.

In M. cerifera, I. cassine, and O. regalis, the total reduction in SI over the CO2 range studied exceeds the average standard deviation. These species are therefore considered to have the highest potential to serve as indicator species for reconstructing atmospheric CO2 concentrations. To independently evaluate the CO2 responsiveness in these species observed at Alligator Crossing, complementary SI data from herbarium leaves are used as modern training sets for generating calibration curves that can be used to infer past CO2 levels from SI values calculated for subfossil leaf remains.

Figure 4A–C shows the relation between SI values of herbarium samples of M. cerifera, I. cassine, and O. regalis and measured historical CO2 concentrations at the year the herbarium specimens were collected. To account for the nonlinear response of SI to changing CO2 concentrations, both the herbarium SI data and the historical CO2 values are log-transformed before fitting a linear response curve through the data sets. For M. cerifera, this results in a relationship of CO2 = 103.1649 – [0.5055 x log(SIfossil)] with a coefficient of determination (R2) of 0.67 between measured and inferred CO2 values and a root mean square error (RMSE) of 13.9 ppmv CO2 (Fig. 4A). For I. cassine (Fig. 4B) and O. regalis (Fig. 4C), the regression curves and error statistics were CO2 = 102,8861 – [0.317 x log(SIfossil)] with R2 = 0.73 and RMSE = 8.9 ppmv CO2 and CO2 = 102.973 – [0.3445 x log(SIfossil)] with R2 = 0.62 and RMSE = 16.36 ppmv CO2, respectively.



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  		Fig. 4. CO2 inference models based on herbarium data and predicted CO2 concentrations from subfossil leaf material. (A–C) Models for CO2 estimations based on herbarium training sets for (A) M. cerifera, (B) I. cassine, and (C) O. regalis measured atmospheric CO2 at sampling date plotted against mean stomatal index (SI) values per sample analyzed. Regressions after log transformation of both SI and CO2, plotted ± 1 root mean square error (RMSE). (D–F) Correlations of measured atmospheric CO2 concentrations at time of deposition at Alligator Crossing and predicted atmospheric CO2 from mean SI values of Alligator Crossing inferred from herbarium models as in Fig. 4 A–C for (D) M. cerifera, (E) I. cassine, and (F) O. regalis; dashed 1:1 lines in D–F visualize deviations of estimates from normality

 
To test the quality of the calibration curves, and thus the accuracy of CO2 estimates, atmospheric CO2 levels are inferred from the SI values of the subfossil material from Alligator Crossing using the herbarium models. In Fig. 4D–F, the inferred CO2 concentrations are plotted over measured historical CO2 levels that correspond to the age of the studied peat samples. The resulting correlations for M. cerifera (Fig. 4D), I. cassine (Fig. 4E), and O. regalis (Fig. 4F) are R2 = 0.81 (P < 0.0001), R2 = 0.59 (P = 0.001) and R2 = 0.26 (P = 0.01), with slopes of the summarizing regressions of 0.80, 0.49 and 0.36, respectively.

DISCUSSION

Analysis of annually accumulating leaf material in lake and peat deposits has been demonstrated to be a highly suitable approach to assess acclimation of leaf characteristics to increasing CO2 (Wagner et al., 1996 ; Kouwenberg et al., 2003 ). In the present study, the SI of all five species examined in the Alligator Crossing peat sequence continuously decreased over the past 60 years, which corresponds to an atmospheric CO2 increase from 310 ppmv to 370 ppmv. The observation confirms that CO2 responsiveness occurs among a variety of typical components of contrasting canopy layers of the hardwood-swamp vegetation of north-central Florida. Apparently this vegetation type is well-ventilated, preventing a buildup of elevated CO2 concentrations at the forest floor during the growing season.

While the upper canopy elements Acer and Quercus are already known to have the capacity to reduce the number of stomata under postindustrial CO2 increase (Woodward, 1987 ; Kürschner et al., 1997 ), a similar pattern is now documented for the first time for the middle canopy elements Myrica and Ilex. Of particular significance is the declining SI of the undergrowth element Osmunda because no information on CO2 responsiveness has so far been available for ferns. The results from Alligator Crossing indicate that this long-lived, deciduous fern obviously possesses a comparable response mechanism as demonstrated for woody seed plants.

Although the general trend in stomatal frequency response is common to all species, the rates of change vary considerably. The weakest response is observed in the two upper canopy species Q. nigra and A. rubrum. Studies on European Quercus species have demonstrated a strong CO2 signature, but the sigmoidal SI response plateaus at 320–340 ppmv CO2 (Kürschner et al., 1997 ). The weak response here obtained for Q. nigra could well be the result of the low number of samples available, in combination with a distribution corresponding to the 310–360 ppmv CO2 range, which seems to comprise the response limit of Quercus leaves. Although the number of samples of A. rubrum is higher, accurate quantification of the SI reduction is hampered by the high intrinsic variability in this species, expressed in the high standard deviation of the SI mean values. For Acer, effects of environmental factors other than CO2 on stomatal frequency have not yet been determined. Notably variation in sun and shade leaves needs consideration. Similar to Quercus, also response limits could be responsible for the weak responsiveness of Acer leaves.

A pronounced decrease in SI values is observed in M. cerifera and I. cassine as well as in O. regalis, for which the mean SI standard deviation is considerably lower than the total SI range over the time period covered in the peat sequence. This would point to a high potential of these species to be indicators for atmospheric CO2 reconstructions. That the observed SI changes are not related to solely local environmental changes at Alligator Crossing is evident from the comparable patterns observed in the herbarium studies, in which leaf samples from all over Florida grown at various localities, were taken into consideration.

The availability of both herbarium material and leaf remains from near-annually dated peat deposits provides the opportunity to estimate the quality of stomata-based prediction models for past atmospheric CO2 concentrations commonly derived from herbarium training sets, only (e.g., Rundgren and Beerling, 1999 ; McElwain et al., 2002 ). In the three herbarium studies (Fig. 4A–C), the comparable R2 values initially indicate a good performance of the regressions through the herbarium data of M. cerifera (R2 = 0.67), I. cassine (R2 = 0.73) and O. regalis (R2 = 0.62) and, thus, a satisfactory quality of the modern training sets. However, when these regression models are applied to the SI values from Alligator Crossing and the inferred CO2 concentrations compared with the actually measured CO2 levels at the time of growth of the subfossil material, significant differences in prediction accuracy become apparent. In I. cassine and O. regalis, correlation coefficients and slope values are relatively low (Fig. 4E, F), denoting unsatisfactory performance of the response models based on the herbarium data sets. These differences in model quality are in first instance related to the properties of the specific training sets based on herbarium data, which emphasizes the necessity for meticulous sample collection when calibration data sets are derived from herbarium training sets only.

The herbarium study for O. regalis reveals very high scatter in the SI values. In addition, the lack of specimens grown under the CO2 range from 330 to 360 ppmv leads to an unequal distribution of the included data points along the CO2 gradient. The cluster of exclusively high SI values observed under 370 ppmv CO2 (this sample from 1998 includes young leaves only) causes a bias to the model and leads to underestimation of the CO2 concentrations inferred from the SI values for subfossil leaf material. Although O. regalis possesses the capacity to respond to changing CO2 levels by adjusting its stomatal frequency, the value of this species for CO2 reconstructions remains uncertain based only on the data presented here.

Similar to O. regalis, the herbarium data set for I. cassine shows an unequal distribution of data points along the CO2 gradient, which is, in this case, mainly due to the very low overall number of samples studied (N = 9). Even though there exists a strong relationship between SI and CO2 in the herbarium material, inferred CO2 concentrations from the subfossil leaf samples indicate that CO2 inferences based on the present training set are problematic, especially towards the higher end of the CO2 range. However, the low intrinsic variability and the relatively high rate of change in this species, corroborate the potential for CO2 reconstructions, given a more extensive analysis of herbarium material.

The results obtained for M. cerifera—a high correlation (R2 = 0.87; Fig. 4D) between measured and predicted CO2 from subfossil material and the regression slope of 0.80—indicate that the model derived from the herbarium data for this species is highly accurate. Even though the number of herbarium samples (N = 19) is still relatively small, the observed scatter is low and the data are equally distributed over both the CO2 and SI ranges. With the high rate of change and the low intrinsic variability in this species, M. cerifera clearly has an exceptionally high potential for atmospheric CO2 reconstructions.

Concluding remarks
This multispecies analysis of fossil leaf material from the Alligator Crossing site demonstrates that stomatal frequency changes are a common response to CO2 changes in different components of plant communities, even though the adaptation rates may differ significantly. Discrimination of potential species for atmospheric CO2 reconstructions and methodical assessment of the CO2 prediction quality of stomatal frequency data is enabled by the combined analysis of herbarium material and the precisely dated subfossil leaf record.

In the present study, the data sets for herbarium and subfossil leaf samples are strictly separated for methodological purposes. However, the overall quality of the models generated for M. cerifera, I. cassine, and O. regalis can be further increased by combination of both data sets. The reliable age assessment for the subfossil material, grown under measured historical CO2 levels, allows this data to be directly used for model regression. By combining herbarium data with data from natural archives, modern training sets can be expanded and the model quality further improved.

Myrica cerifera and I. cassine are two widely distributed and very common species in the southeastern United States. By adding them to the group of practicable species for CO2 reconstructions, the application range of the stomatal frequency proxy is successfully extended into the warm-temperate to subtropical realm of North America.

FOOTNOTES

1 We thank T. van Hoof and T. van Druten for field assistance and W. Kürschner, T. Donders, L. Kouwenberg, O. Heiri, T. Lott, and two reviewers for comments on the manuscript. The help of K. Perkins in selecting the FLAS herbarium samples is gratefully acknowledged. This report is Netherlands Research School of Sedimentary Geology publication no. 20040504, and no. 576 in the series University of Florida Contributions to Paleontology. Back

4 Author for correspondence (e-mail: r.wagner{at}bio.uu.nl ) Back

LITERATURE CITED

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