Physiological Responses of Beech and Sessile Oak in a Natural Mixed Stand During a Dry Summer

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1 Annals of Botany 89: 723±730, 2002 doi: /aob/mcf133, available online at Physiological Responses of Beech and Sessile Oak in a Natural Mixed Stand During a Dry Summer YANNIS RAFTOYANNIS and KALLIOPI RADOGLOU* Forest Research Institute, Vasilika, 57006, Thessaloniki, Greece Received: 23 November 2001 Returned for revision: 12 January 2002 Accepted: 4 March 2002 Responses of CO 2 assimilation and stomatal conductance to decreasing leaf water potential, and to environmental factors, were analysed in a mixed natural stand of sessile oak (Quercus petraea ssp. medwediewii) and beech (Fagus sylvatica L.) in Greece during the exceptionally dry summer of Seasonal courses of leaf water potential were similar for both species, whereas mean net photosynthesis and stomatal conductance were always higher in sessile oak than in beech. The relationship between net photosynthesis and stomatal conductance was strong for both species. Sessile oak had high rates of photosynthesis even under very low leaf water potentials and high air temperatures, whereas the photosynthetic rate of beech decreased at low water potentials. Diurnal patterns were similar in both species but sessile oak had higher rates of CO 2 assimilation than beech. Our results indicate that sessile oak is more tolerant of drought than beech, due, in part, to its maintenance of photosynthesis at low water potential. ã 2002 Annals of Botany Company Key words: Sessile oak, Quercus petraea ssp. medwediewii, beech, Fagus sylvatica L., CO 2 assimilation, stomatal conductance, leaf water potential, drought. INTRODUCTION Water availability is a major factor limiting the occurrence, abundance and growth of trees (Woodward, 1987). The scenario of climate change in SE Europe predicts increased air temperatures and reduced rainfall. If this occurs, the current distribution of plant communities will change (Friend et al., 1996). Differences among species in rooting depth, leaf morphology, leaf water potential, osmotic potential, photosynthesis and stomatal conductance are involved, to varying extents, in determining how a species responds to drought. This response, ultimately, determines the growth, reproduction and distribution of species, and the composition of vegetation. Stomatal control is the rst, and perhaps most important, step in the response to drought, as decreased stomatal conductance reduces the rate of water loss, slows the rate of development of water stress and minimizes its severity. Photosynthesis is a physiological process that has farreaching effects on plant performance. It is strongly affected by water shortage as reduced stomatal conductance generally decreases photosynthetic CO 2 assimilation. Smaller stomatal conductance, whilst possibly resulting in less severe water stress and so preventing or decreasing damage to the photosynthetic mechanisms (as well as other metabolic processes), may decrease CO 2 assimilation. The relationship between water stress, stomatal conductance and photosynthesis is therefore an important aspect of stress tolerance (Dickson and Tomlinson, 1996). Decreasing soil water content is ultimately responsible for drought-induced stomatal closure of woody plants (Jarvis and Sandford, * For correspondence. Fax , radoglou@ spark.net.gr 1986) and drought-tolerant species are able to maintain higher gas exchange than those less tolerant (Ni and Pallardy, 1991). Thus, to predict how species may respond to changing water supply as a consequence of climate change, it is necessary to understand the mechanisms by which different species respond to drought. In Greece, oak and beech forests, sometimes as mixed stands, are the most extensive broad-leaved forests, producing valuable hardwood timber as well as being invaluable for wildlife and protecting water catchments. In recent years, we have observed that beech shows symptoms of leaf discoloration, or even leaf fall, in mid-summer, while sessile oak trees remain in good condition throughout the summer. Drought has been suggested as a major factor responsible for the decline in beech and oak reported in Europe in recent decades (Innes, 1992). Even a slight reduction in drought tolerance could contribute to a long-term decline, and may lead to loss of beach relative to oak. Indeed, Peterken and Mountford (1996) found that following the 1976 drought in Britain, the growth rate of damaged beech trees was negligible for 12 years and never fully recovered. In this paper, we attempt to explain the eld observations of changes in the appearance and the decreased vigour of beech compared with sessile oak, and we assess the possible effects of drought induced by climate change. We focus on the responses of a naturally occurring mixed stand of beech (Fagus sylvatica L.) and sessile oak [Quercus petraea ssp. medwediewii (A. Camus) Menitsky (Q. dalechampii Ten.)] to one of the most extreme droughts recorded in Greece, which occurred during the summer of We assessed the photosynthetic performance of leaves of both species under drought conditions. Species comparisons in mixed stands are not well documented and better knowledge of the ã 2002 Annals of Botany Company

2 724 Raftoyannis and Radoglou Ð Tree Physiology in a Mixed Beech±Oak Forest physiological responses to environmental limitations is necessary for understanding the successional status of those species and the composition of mixed stands, as well as the long-term responses to drought. Furthermore, data on net photosynthesis rates and stomatal behaviour under eld conditions are necessary to answer basic questions on how ef ciently environmental resources, in particular, water, are used for primary production. Such information is also potentially useful for modelling responses of forests to environmental conditions. As Hinckley et al. (1981) suggested, observations of tree responses to extreme drought events often prove useful indicators of possible drought-tolerance mechanisms. Although the physiological responses of beech and oak populations in central Europe to drought are relatively well studied, very few studies have dealt with beech populations at the southern limit of their range, and there are no reports of the water relations of Quercus petraea ssp. medwediewii (A. Camus). Site description MATERIALS AND METHODS Sessile oak [Quercus petraea ssp. medwediewii (A. Camus) Menitsky (Q.dalechampii Ten.)] and beech (Fagus sylvatica L.) (Schwarz, 1964; Christensen, 1997) were studied in the 1998 growing season in a mixed open woodland located on Mount Vertiscos (23 18 E, N), 70 km north of Thessaloniki, Greece, at an elevation of 900 m. The climate is transitory between Mediterranean and temperate, Csb according to the KoÈppen classi cation system, with a mean annual temperature of 12 C and mean annual rainfall of 810 mm (data from 1975 to 1997). During the experiment, environmental conditions were monitored using an automated weather station located in a forest clearing near to the trees studied. Air temperature, relative humidity, soil moisture (at 30 cm depth) and precipitation were recorded every 30 min with sensors connected to a data-logger (DL2 Delta-T Logger; Delta-T Devices Ltd, Cambridge, UK). Leaf measurements Sampled sessile oak trees had an average height of 6 m and beech of 9 m. Two typical trees of each species, growing less than 10 m apart and experiencing the same microtopographical and soil conditions, were selected at random for measurements. Water potential of leaves (Y) was measured according to Scholander et al. (1965) using a pressure chamber (Wescor Inc., Logan, UH, USA). Net CO 2 assimilation rate (A) stomatal conductance (g s ) and intercellular CO 2 concentration (C i ) were measured and calculated with a portable gas exchange system (LI-6400; Li-Cor Inc., Lincoln, NE, USA). Air temperature (T a ), vapour pressure de cit (VPD), relative humidity (RH) and photosynthetic active radiation (PAR) were recorded simultaneously close to the leaf surface. All variables were measured on ve fully expanded leaves per tree, selected at random in the south-oriented, middle crown, between 1000 and 1200 h every 14 d from June to September Diurnal courses of the physiological variables were measured at 2 hourly intervals from 0800 h on 17 June, 13 July, 6 August and 17 September. Data analysis Differences in measured variables between dates and species were analysed by ANOVA, and means were compared with Tukey's multiple comparisons tests. All tests for signi cance were conducted at P < 0 05, unless otherwise indicated. Regression analysis was performed using the mean values of variables. Site environmental conditions RESULTS Seasonal changes in environmental conditions within the woodland are shown in Fig. 1. Mean daily air temperature uctuated around 20 C in June±August, becoming cooler in September. Periods of heavy rain occurred at the beginning of June, followed by a period of virtually no rain until early September when more frequent rainfall occurred. Soil moisture at 30 cm depth rose to 45 % after the high rainfall early in the season and dropped below 10 % from the end of June until the end of September. Relative humidity was between 40 and 60 % during the summer months, increasing to 85 % in September. FI G. 1. Seasonal courses of relative humidity (RH, dotted line), air temperature (T a, continuous line), soil moisture at 30 cm depth (circles), and rainfall (bars) from 1 June to 1 Oct Seasonal patterns Beech and sessile oak had a similar Y during the season (Fig. 2A) with no signi cant differences between species at any time. Both species had a high water potential at the beginning of June (Y greater than ±2 MPa), which then dropped sharply until the beginning of July, after which it was relatively constant at ±4 MPa until the end of August.

3 Raftoyannis and Radoglou Ð Tree Physiology in a Mixed Beech±Oak Forest 725 Photosynthetic CO 2 assimilation for oak leaves increased from a mean of 11 mmol m ±2 s ±1 in early June to 22 mmol m ±2 s ±1 in early July and then decreased slowly to 12 mmol m ±2 s ±1 at the end of September (Fig. 2B). Assimilation of beech leaves was small (mean 6 3 mmol m ±2 s ±1 ) at the beginning of June, reached its peak in mid-june and then decreased progressively with some signi cant uctuations (lowest point 3 2 mmol m ±2 s ±1 ). There was no signi cant difference in A between the species on days 2, 3 and 12. Trends for stomatal conductance were similar for both species except on day 12 (Fig. 2C). Initial values of g s for both species were between 150 and 200 mmol m ±2 s ±1 and were not signi cantly different. Values then increased up to 290 mmol m ±2 s ±1 for oak and 250 mmol m ±2 s ±1 for beech, followed by a gradual and continuous reduction until the end of September, with minimum values of 65 and 30 mmol m ±2 s ±1 for oak and beech, respectively. Mean values of g s were always greater for oak than for beech. The relationship between A and g s was positive and linear for both species, but was signi cant only for oak (oak A = g s , R 2 = 0 54; beech A = g s , R 2 = 0 87) (Fig. 3A). Assimilation of oak increased with increasing vapour pressure de cit, while A for beech stabilized and started decreasing above 2 kpa (oak A = ± VPD VPD , R 2 = 0 49; beech A = ±1 472 VPD VPD , R 2 = ) (Fig. 3B). Both species responded similarly to light intensity: A increased up to 1500 mmol m ±2 s ±1 and then decreased above it (oak A = ±3E-05 PAR PAR ± 44, R 2 = 0 39; beech A = ±2E-05 PAR PAR ± 39, R 2 = 0 21) (Fig. 3C). A signi cant and positive linear relationship was found between A and temperature for oak, while assimilation decreased above 32 C in beech (oak A = T a ± 4 24, R 2 = 0 83; beech A = ± T a T a ± , R 2 = 0 38) (Fig. 3D). The reduction in Y was followed by a reduction in A in beech trees but not in sessile oak (oak A = ± Y 2 ± Y ± , R 2 = 0 28; beech A = Y , R 2 = 0 31) (Fig. 3E). The relationship between C i and A was linear for both species, but A of oak leaves was more than double that of beech at the same C i (oak A = C i , R 2 = 0 62; beech A = C i ± 2 92, R 2 = 0 58) (Fig. 3F). The relationship between g s and Y was similar to that of A and Y for both species (oak g s = ±31 655Y 2 ± Y ± , R 2 = 0 09; beech g s = Y + 379, R 2 = 0 68) (Fig. 4). F I G. 2. Seasonal courses of midday leaf water potential (Y) (A), CO 2 assimilation rates (A) (B) and stomatal conductance (g s ) (C) of beech (open circles) and oak (closed circles) trees. Data are means 6 1 s.d. (n = 10). Diurnal patterns On 17 June, the largest average value of A for oak (17 4 mmol m ±2 s ±1 ) occurred at 1700 h, while mean values measured at other times of the day were above 14 mmol m ±2 s ±1 and did not differ signi cantly from each other (Fig. 5). On the same day, beech followed the same diurnal pattern of mean A, but with lower rates at all times (the largest average value, 14 6 mmol m ±2 s ±1, being recorded at 1000 h). On 13 July, A was high in the morning for oak, decreased sharply at midday and then increased again but not to the morning values. Beech responded similarly. On 6 August, mean A for oak was 16 5 mmol m ±2 s ±1 in the early morning, declined at midday and remained relatively

4 726 Raftoyannis and Radoglou Ð Tree Physiology in a Mixed Beech±Oak Forest F I G. 3. Relationships over the period from June to October, between CO 2 assimilation rates (A) and stomatal conductance (g s ) (A), vapour pressure de cit (VPD) (B), photosynthetic active radiation (PAR) (C), air temperature (T a ) (D), midday leaf water potential (Y) (E), and intercellular CO 2 concentration (C i ) (F) of beech (open circles) and oak (closed circles) trees. Data represent means 6 1 s.d. (n = 10) of seasonal observations. F I G. 4. Relationship between the stomatal conductance (g s ) and midday leaf water potential (Y) of beech (open circles) and oak (closed circles) trees. Data represent means 6 1 s.d. (n = 10) of seasonal observations. constant until 1900 h after which it decreased. Beech trees followed the same pattern but with lower values of A. On 17 September, mean values of A for oak were smaller than those measured previously, even before 1000 h; they declined thereafter with some recovery at 1700 h. Values of A for beech were also smaller than previously, and they declined continuously throughout the day. In general, stomatal conductance followed similar patterns to A, with mean values ranging from 32 to 272 mmol m ±2 s ±1 for oak and from 1 to 252 mmol m ±2 s ±1 for beech (Fig. 6). Stomatal conductance declined progressively through the day and as drought progressed for both species; however, g s of beach decreased much more than that of oak. When mean values of A were plotted against mean values of g s, positive logarithmic relationships were found for both species (oak A = ln(g s ) ± , R 2 = 0 83; beech A = ln(g s ) ± , R 2 = 0 77) (Fig. 7A). Vapour pressure de cit did not signi cantly affect assimilation rates in oak or beech (oak A = ±1 026VPD , R 2 = ; beech A = ±1 512VPD , R 2 = 0 09) (Fig. 7B). Carbon assimilation for both species increased with increasing light intensity up to 1000 mmol m ±2 s ±1, and then the rate of increase slowed (oak A = ln (PAR) ± , R 2 = 0 13; beech A = ln (PAR) ± , R 2 = 0 03) (Fig. 7C). Assimilation rates for both species were limited at temperatures below 27 C and above 35 C, although the effect was not signi cant (oak A = ± T a T a ± , R 2 = 0 09; beech A = ± T a T a ±

5 Raftoyannis and Radoglou Ð Tree Physiology in a Mixed Beech±Oak Forest 727 F I G. 5. Diurnal time courses of CO 2 assimilation rates (A) of beech (open circles) and oak (closed circles) trees, on 17 June, 13 July, 6 Aug. and 17 Sep Data represent means 6 1 s.d. (n = 10). F I G. 6. Diurnal time courses of stomatal conductance (g s ) of beech (open circles) and oak (closed circles) trees on 17 June, 13 July, 6 Aug. and 17 Sep Data represent means 6 1 s.d. (n = 10).

6 728 Raftoyannis and Radoglou Ð Tree Physiology in a Mixed Beech±Oak Forest F I G. 7. Relationships over the diurnal time course at the different periods of measurement, between CO 2 assimilation rates (A) and stomatal conductance (g s ) (A), vapour pressure de cit (VPD) (B), photosynthetic active radiation (PAR) (C), air temperature (T a ) (D), and intercellular CO 2 concentration (C i ) (E) of beech (open circles) and oak (closed circles) trees. Data represent means 6 1 s.d. (n = 10) of diurnal observations , R 2 = 0 22) (Fig. 7D). The relationship between C i and A was linear for both species but that of oak was greater than that of beech at the same C i (oak A = C i , R 2 = 0 39; beech A = C i ± 2 07, R 2 = 0 70) (Fig. 7E). DISCUSSION The year in which the study was conducted was particularly dry and the trees experienced drought stress. Annual rainfall in 1998 was 520 mm, much lower than the mean annual rainfall (810 mm) for the period 1975±1997. In 1998, July and August were very dry, with only 2 and 11 mm of rain, respectively, compared with an average of 52 and 50 mm rain in these months over the period 1975±1997. As a result, soil moisture was around 5 % for July±September. In both oak and beech, Y was below ±3 0 MPa after 1 July, indicative of rather severe water stress. Similar results have been reported for beech and oak by Aranda et al. (1996) and for four Mediterranean oaks by Fotelli et al. (2000). Beech and oak are considered to be under stress when Y falls below ±2 0 MPa (Breda et al., 1993), and twigs of oak were found to lose turgor around ±3 0 MPa (Dreyer et al., 1990). Although the seasonal pattern of Y was remarkably similar for both species, A and g s were signi cantly lower for beech than for oak for most of the measurement dates. Similar results were reported for beech and for Q. petraea ssp. petrae by Aranda et al. (2000) and Backes and Leuschner (2000). Sessile oak responded to drought with a gradual reduction of A and g s, but they remained substantial even when water de cits were strong. Similarly, severely water-stressed Q. petraea trees still exhibited substantial CO 2 uptake rates at midday (Epron and Dreyer, 1990; Epron and Dreyer, 1993). The stomatal conductance of Q. petraea seedlings remained almost unaffected by drought, and the ratio of leaf to ne-root biomass was signi cantly diminished in drought-stressed seedlings (Thomas and Gausling, 2000). On the other hand, water stress signi cantly decreased A and g s of beech, as also observed by Tognetti et al. (1994). Thomas (2000) found that drought-stressed beech seedlings developed more visible symptoms of damage, and faster, than oak seedlings: oak adapted to drought by reducing the leaf : root ratio, and the number of second ushes and buds. Drought not only decreased A and g s but also changed the diurnal patterns of gas exchange. Well-watered plants in a

7 Raftoyannis and Radoglou Ð Tree Physiology in a Mixed Beech±Oak Forest 729 temperate climate show a dome-shaped diurnal course of A, paralleling the course of global radiation (Tenhunen et al., 1987). In hotter and drier conditions, as at our experimental site, this pattern changes. In June, the diurnal course of A followed the typical pattern of midday depression which has also been reported for oak by Epron et al. (1992). In July, August and September, A was greatest in the morning and did not recover to the morning values following the midday depression. The same afternoon decline in A was observed in the Mediterranean species Arbutus unedo (Tenhunen et al., 1982) and Cistus salvifolius (Harley et al., 1987). Such changes in the diurnal patterns of A can be attributed to greater sensitivity of leaf gas exchange to T a and VPD under drought stress (Tenhunen et al., 1987). In our study, the reduction in A was accompanied by a reduction in C i for both species, which indicates stomatal inhibition of photosynthesis. Epron and Dreyer (1990) observed similar results for sessile oak trees subjected to short-term drought, but when trees were subjected to longterm drought they maintained high C i, suggesting nonstomatal control of A. Furthermore, oak showed higher A than beech at the same C i, suggesting that the photosynthetic system of oak is less affected by drought stress. The strong positive relationship between A and g s for both seasonal and diurnal courses suggests that stomatal closure was the main factor affecting CO 2 assimilation. The relationships between A and g s were linear for the seasonal data, but logarithmic for the daily data. Stomatal regulation of leaf gas exchange during water shortage has been well documented for drought-adapted species, and similar linear relationships between A and g s have been observed (Schulze and Hall, 1982; Epron and Dreyer, 1993). However, many other environmental variables, such as irradiance, temperature and vapour pressure de cit, may interact with soil water depletion and cause a reduction in photosynthesis and alteration of the linear relationship between A and g s (Epron and Dreyer, 1990; Triboulot et al., 1996). In conclusion, our results show that CO 2 assimilation of leaves of Quercus petraea ssp. medwediewii (A. Camus) Menitsky is more tolerant to drought stress than that of Fagus sylvatica L. This is the rst report on gas exchange of Quercus petraea ssp. medwediewii (A. Camus). The Y of both species was the same throughout the drought, suggesting that supply and loss of water were similar in the two tree species in a mixed stand. Stomatal control was the main response of both tree species to drought. When trees were unstressed, stomatal conductance was similar in both oak and beech, but, during the dry period, stomatal conductance of oak remained much higher than that of beech. Consequently, oak, which had higher rates of A than beech when not stressed at the same C i, maintained higher rates of A than beech. This suggests that the photosynthetic metabolism of beech is more sensitive to low Y: this could be a consequence of differences in water content, or osmotic adjustment. From this knowledge of gas exchange during water shortage, we predict that oak will predominate in forest communities as drought becomes more common and severe. The information provides a basis to forecast the successional status of individual species and changes in communities. ACKNOWLEDGMENTS We thank the European Commission for providing funds to conduct this research, supported by the FAIR Programme, contract no: FAIR1 CT95±497. 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