Atmospheric vs soil water deficit as leaf conductance regulator in Mediterranean trees : a correlational approach

Orsis 10, 1995 43-50 Atmospheric vs soil water deficit as leaf conductance regulator in Mediterranean trees: a correlational approach Carles Castell and Jaume Terradas Universitat Autbnoma de Barcelona Centre de Recerca Ecolbgica i Aplicacions Forestals 08193 Bellaterra (Barcelona). Spain Tel. number: 34-3-5812028. Fax number: 34-3-581 1321 Abstract Both soil and atmospheric water deficits have been considered as the main variable determining stomatal closure in native Mediterranean species in the field, depending on the species and places studied. In this study, field data on leaf conductance of Arbutus unedo, a shallow-rooted tree, correlates higher with the predawn leaf water potential than leaf conductance of Quercus ilex, a deeprooted tree. Leaf conductance of mature individuals of both species correlates higher with vapour pressure deficit than leaf conductance of resprouts, which have lower leaf area. Data presented suggest that the relationship between root depth and leaf area in each individual could determine the relative importance of soil water deficit and vapour pressure deficit on controlling leaf conductance. Key words: Arbutus unedo, Quercus ilex, root: shoot ratio, leaf conductance, water balance. Resum. Importancia relativa del d2ficit hídric del sol i de l'atmosfera sobre la regulació estomritica en arbres mediterranis: una aproximació correlacional Segons les esptcies i els indrets considerats, tant el dtficit hídric atmosftric com el dtficit hídric del sbl han estat considerats com la variable principal que determina el tancament estomitic en esptcies mediterrinies en condicions de camp. En aquest estudi, la conductbcia foliar obtinguda al camp en Arbutus unedo, una esptcie d'arrels superficials, esta més correlacionada amb el potencial hídric a l'alba que la conducthcia foliar de Quercus ilex, que presenta un sistema radicular més profund. D'altra banda, la conductincia foliar dels individus adults de les dues esptcies esta més correlacionada amb el dtficit de pressió de vapor que la conductincia foliar dels rebrots de les mateixes esptcies, que tenen una menor hea foliar. Les dades presentades suggereixen que la relació entre la profunditat de les arrels i l'irea foliar en cada individu podria determinar la importincia relativa del dtficit hídric del sbl i del dtficit de pressió de vapor sobre el control de la conductbcia foliar. Paraules clau: Arbutus unedo, Quercus ilex, proporció parts atriestparts subterrbies, conductincia foliar, balanc; hídric. 44 Orsis 10, 1995 Carles Castell and Jaume Terradas Introduction Although stomatal responses to environmental changes are quite well understood for plants growing in growth-chambers and greenhouses experiments, there is less certainty about the factors controlling stomatal conductance in natural vegetation growing in field conditions. Three mechanisms of stomatal response to atmospheric or soil water deficit have been described (Ludlow, 1980; Farquhar and Sharkey, 1982; Schulze and Hall, 1982; Schulze, 1986): direct response of stomata to air humidity, response through changes in mesophyll water status as a hydraulic signal, and response to soil water deficit through a chernical root signal. The mechanisms and the relative contribution of each process to controlling stomatal conductance are still uncertain (Kramer, 1988; Schulze et al., 1988). In native Mediterranean species, evidence has been presented to support the dominance of one or other of these mechanisms, depending on species and places. Tenhunen et al. (1987) showed that stomatal conductance was more clearly related to soil rather than leaf water potential in severa1 Mediterranean trees and shrubs; data presented by Crombie et al. (1987) in Eucalyptus marginata, Morrow and Mooney (1974) in Heteromeles arbutifolia and Arbutus menziesii, and Gollan et al. (1985) in Nerium oleander, support this dependency of stomata on soil water content. On the other hand, leaf water status was described by Roberts et al. (198 1) as the main inducer of stomatal closure in some species of the chaparral. Greater importance of soil water potential in relation to vapour pressure deficit was indicated in Eucalyptus globulus by Pereira et al. (1987). However, Turner et al., (1984) in Arbutus unedo and Nerium oleander, and Beadle et al. (1985) in Pinus sylvestris, showed the dominant effect of vapour pressure deficit on conductan- ; ce, both directly on the leaf epidermis and through leaf water potential. The objective of this study was to test the relative importance of soil and atmospheric water deficit on the regulation of leaf conductance in contrasting situations, using a correlational approach. Results were obtained for nature plants and resprouts of Arbutus unedo and Quercus ilex, two woody Mediterranean trees. Resprouts have a lower leaf area than mature plants, and Q. ilex individuals have deeper roots than A. unedo. Thus, we may assess the stomatal response among plants with very dissimilar relationship between leaf area and root depth. Although the correlational approach can not be used to provide evidence for mechanisms involved in the regulation of stomata, the results may help to understand the response of stomata to the environmental conditions and their ecological implications. Materials and methods The study site is located at an elevation of 350 m, on a Southern slope (15-20") of the Collserola Natural Park in Northeast Spain, very close to Barcelona (41" 25' 25" N, 2" 6' 30" E). The vegetation burned in the summer of 1973. The plant canopy during the study period was near closure, dominated by Arbutus unedo L., Quercus ilex L. and Pinus halepensis Mill. During the sarnpling year (June 1990 - May 1991), total rainfall was 940 rnm (mean 725 mm). The dry period occurred in July and August, when there were only 29 mm of rainfall (Figure 1). Leaf Conductance Regulation Orsis 10. 1995 45 JJASONDJFMAM Month 46 Orsis 10, 1995 Carles Castell and Jaume Terradas Mean annual temperature was 13.6 "C. The soil is a very shallow (19 + 1 cm, n = 18), loamy clay developed on Palaeozoic schists with a very low water storage capacity (lithic xerorthent). ~hes~ecies considered were A. unedo, a laurophyiious shallow-rooted tree and Q. ilex, a schlerophyllous deeprooted tree. Plants of Arbutus unedo selected for study were on the average 3 meters in height and 5 meters in diameter, with three to five main stems. Excavated root systems of A. unedo individuals at the study site were restricted to the 20 cm thick soil layer and never penetrated the bedrock. Plants of Quercus ilex were on the average 4 meters in height and 4 meters in diameter, with three to five main stems per individual. Tap roots of Q. ilex penetrated the bed-rock and still had a diarneter of greater than 4 cm at the maximum depth we were able to observe (approx. 50 cm). En both species, three individuals were cut down on 7 May 1990 to produce resprouts, and three more individuals were left as mature plants. In addition, six more A.unedo plants, three resprouted and three mature, were watered during the summer drought (July and August). In all plants, leaf conductance was measured at midday with a porometer (ADC Ltd., model LCA-2, Hoddesdon, UK); predawn leaf water potentia1 (PWP), as an indicator of soil water deficit, was measured with a pressure chamber (Soil Moisture Inc., model 3005, Santa Barbara, CA, USA); additionally, we calculated the midday vapour pressure deficit (VPD) in order to use it as a atmospheric water deficit indicator. Samples were taken weekly during the surnmer, and approximately every month during the rest of the year, fiom June 1990 to May 1991. For each group of plants, regressions were performed between midday leaf conductance over the whole year as the dependent variable, and daily values of PWP and VPD as the independent variables. The regression used was the one showing the highest coefficient of deterrnination: power regression for PWP-conductan- ce, and linear regression for VPD-conductance. Regressions were characterized by their standardized regression coefficient (Beta coefficient, Norusis, 1985). Beta coefficient permit us to compare the effect of different independent variables removing the effect of unities; higher values of Beta indicate greater response of leaf conductance to changes in the independent variable. Results and discussion Decreases in leaf water potential and leaf conductance in resprouts and mature plants of both species occurred rapidly after the onset of summer drought and recovered after heavy rains of late-Summer (Figure 2), as typically observed previsusly at other sites (Tenhunen et al., 1985). These data are largely discussed in two previous papers (Castell and Terradas, 1994; Castell et al.,1994). Beta coefficients obtained for the regressions in each group of individuals are graphically represented in the figures 3 and 4. A. unedo and Q. ilex individuals show similar values of Beta for VPD-conductance regression, but Beta values for PWP-conductance regression are much higher in A. unedo (Figure 3). On the one hand, similar leaf area in individuals of both species may be the reason to explain the similar response of conductance to atmospheric water deficit; on the other hand, the deeper root system of Q. ilex individuals probably leads to a weaker con- Leaf Conductance Regulation Orsis 10, 1995 47 Predawn Water Potential Midday Leaf Conductance Mpa mol m-2 S-' Figure 2. Seasonal course of the predawn leaf water potential (top) and midday leaf conductance (bottom) of mature plant and resprout leaves of A. unedo (left panel) and Q. ilex (right panel) in the field from June 1990 to May 1991. Mature -t ; Resprouts + . 48 Orsis 10, 1995 Carles Castell and Jaume Terradas ductance correlation with soil water deficit than in the more shallow-rooted A. unedo individuals. In the case of resprouts vs. mature plants, resprouts show lower values of Beta for VPD-conductance regression in both species, and also a lower value for PWP-conductance regression in Q. ilex. The weaker conductance correlation with atmospheric water deficit in resprouts is probably related to their lower leaf area. Watering treatment basically involves a decrease of Beta values for PWP- conductance regression, both in A. unedo resprouts and mature plants (Figure 4). Thus, an increase in soil water availability causes conductance correlation with soil water status to decrease. In surnrnary, leaf conductance of each group of individuals seems to show higher correlation with soil or atmospheric water deficit, depending on which is the more limiting. In addition to soil water status and VPD existing at a given tirne and place, on an individual level, the relationship between root depth and leaf area could also determine the relative importance of soil and atmospheric water deficit. So, A. unedo resprouts, with low soil water availability and low transpiring area, are more limited by soil water availability than by vapour pressure deficit. On the contrary, mature individuals of Q. ilex, with a deep root system but also with a high leaf area, are more limited by atmospheric water deficit and less limited by soil water deficit than A. unedo resprouts. In conclusion, water balance in the plant depends on input. I by root absorption, and output water flow by leaf transpiration. Data presented here suggest that the abiotic factor controlling each flow, soil and atmospheric water deficit, may be the main variable determining leaf conductance, depending on which is the most limiting in the water balance of each individual. 1 - al 0.8 m + - 3. I ' -0 5 0.6 L Qi M Au M O 0.2 0.4 0.6 0.8 1 Beta Coef. PWP-Conductance Figure 3. Beta values corresponding to the regressions between predawn water potentia1 and leaf conductance (x axis), and vapour pressure deficit and leaf conductance (y axis), in the different groups of individuals (Qi M = Mature plants of Q. ilex; Qi R = Resprouts of Q. ilex; Au M = Mature plants of A. unedo; Au R = Resprouts of A. unedo). S a > % 0.4 S m .- ,. 0.2 o - - Au R Qi R I I I Leaf Conductance Regulation Orsis 10, 1995 49 Acknowledgements This study was supported by the INIA projects nos. 6072 and FOR91-1054. The study site was put at our disposa1 by the Patronat Metropolita Parc de Collserola. References Beadle, C.L.; Jarvis, P.G.; Talbot, H.; Neilson, R.E. 1985. Stomatal conductance and photosynthesis in a mature scots pine forest. 11. Dependence on environmental variables of single shoots. J. App. Ecol. 22: 573-586. Castell, C.; Terradas, J. 1994. Effects of water and nutrient availability on water relations, gas exchange and growth rate of mature plants and resprouts of Arbutus unedo L. Ann. Bot. 73: 595-602. Castell, C.; Terradas, J.; Tenhunen, J.D. 1994. Water relations, gas exchange, and growth of resprouts and mature plant shoots of Arbutus unedo L. and Quercus ilex L. Oecologia 98: 201-21 1. Crombie, D.S.; Tippett, J.T.; Gorddard, D.J. 1987. Water relations of root-pruned jarrah (Eucalyptus marginata Donn ex Smith) saplings. Aust. J. Bot. 35: 653-663. Farquhar, G.D.; Sharkey, T.D. 1982. Stomatal conductance and photosynthesis. Ann. Rev. Pl. Physiol. 33: 317-345. Gollan, T.; Turner N.C.; Schulze, E.-D. 1985. The responses of stomata and leaf gas exchange to vapour pressure deficits and soil water content. 11. In the sclerophyllous woody species Nerium oleander. Oecologia 65: 356-362. Kramer, P.J. 1988. Changing concepts regarding plant water relations. Plant, Cell & Environ 11: 565-568. M Wat M Unw Watering 4 R Unw R Wat o 1 I I 1 O 0.2 0.4 0.6 0.8 1 Beta Coef. PWP-Conductance Figure 4. Effect of watering on the Beta values corresponding to the regressions between predawn water potentlal and leaf conductance (x axis), and vapour pressure deficit and leaf conductance 0, axis), in resprouts and mature individuals of A. unedo (M Wat = Watered mature plants; R Wat = Watered resprouts; M Unw = Unwatered mature plants; R Unw = Unwatered resprouts). 50 Orsis 10, 1995 Carles Castell and Jaume Tenadas Ludlow, M.M. 1980. Adaptative significance of stomatal responses to water stress. In: N.C. Tumer; P.J. Kramer (eds.) Adaptation of plants to water and high temperature stress. John Wiley & Sons. New York, p. 123-138. Morrow, P.A.; Mooney, H.A. 1974. Drought adaptations in two Californian evergreen sclerophylls. Oecologia 15: 205-222. Norusis, M.J. 1985. SpSSX Advanced Statistics Guide. McGrawHill. New York. Pereira, J.S.; Tenhunen, J.D.; Lange, O.L. 1987. Stomatal control of photosynthesis of Eucalyptus globulus Labill. trees under field conditions in Portugal. J. Exp. Bot. 38: 1678-1688. Roberts, S.W.; Miller, P.C.; Valamanesh, A. 1981. Comparative field water relations of four co-ocumng chaparral shrub species. Oecologia 48: 360-363. Schulze, E.-D. 1986. Carbon dioxide and water vapour exchange in response to drought in the atmosphere and in the soil. Ann. Rev. Plant Physiol37: 247-274. Schulze, E.-D.; Hall, A.E. 1982. Stomatal responses, water loss and C02 assimilation rates of plants in contrasting environrnents. In: O.L. Lange; P.S. Nobel; C.B. Osmond; H. Ziegler (eds.) Encyclopedia of Plant Physiology, New Series, Vol. 12B. Springer- Verlag. Berlin, p. 18 1-230. Schulze, E.-D.; Steudle, E.; Gollan, T.; Schurr, U. 1988. Response to Dr. P.J. Krarner's article, c<Changing concepts regarding plant water relations,, volume 11, number 7. Plant, Cell & Environ 11, p. 565-568. Tenhunen, J.D.; Lange, O.L.; Harley, P.C.; Beyschlag, W.; Meyer, A. 1985. Limitations due to water stress on leaf net photosynthesis of Quercus coccifera in the Portuguese evergreen scrub. Oecologia 67: 23-30. Tenhunen, J.D.; Pearcy, R.W.; Lange, O.L. 1987. Diurnal variations in leaf conductance and gas exchange in natural environments. In: E. Zeiger; G. Farquar; I. Cowan (eds.) Stomatal function. Stanford University Press. Stanford, p. 323-351. Turner, N.C.; Schulze, E.-D.; Gollan, T. 1984. The responses of stomata and leaf gas exchange to vapour pressure deficits and soil water content. I. Species comparison at high soil water contents. Oecologia 63: 338-342. Manuscript received on March 1995