Stomatal behaviour in an oak canopy

Agricultural and Forest Meteorology, 43 (1988) 99-108

99

Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

S T O M A T A L B E H A V I O U R IN A N OAK C A N O P Y

A.J. DOLMAN and G.J. VAN DEN BURG

Department of Physical Geography and Soil Science, State University of Groningen, Melkweg 1, 9718 EP Groningen (The Netherlands) (Received January 19, 1987; revision accepted December 8, 1987)

ABSTRACT Dolman, A.J. and van den Burg, G.J., 1988. Stomatal behaviour in an oak canopy. Agric. For. Meteorol., 43: 99-108. Measurements of stomatal conductance in an oak canopy (Quercus robur) in The Netherlands are described. Diurnal changes in conductance were found to be dependent on solar radiation and vapour pressure deficit. A model describing these relationships was derived from the observed data. Model performance was rather poor, possibly as a result of the neglect of leaf water potential influences on stomatal conductance. A simple approximation for this influence is suggested and discussed.

INTRODUCTION

The sensitivity of the P e n m a n - M o n t e i t h estimates of actual evaporation of forests depends less on the climatological conditions than on appropriate values of the aerodynamic and canopy conductance parameters (Beven, 1979). Knowledge of these conductances is thus a preliminary to any modelling of the water consumption of forested watersheds. In an earlier paper, Dolman (1986) analysed seasonal variation in aerodynamic parameters of an oak canopy (Quercus robur) and discussed the effects on evaporation of intercepted rainfall. The present paper is concerned with variation in stomatal conductance of the same forest. The development of portable porometers in recent years has enabled researchers to investigate fluctuations of stomatal conductance in response to changing environmental conditions in the field. Examples of this approach can be found in Jarvis (1976), Beadle et al. ( 1985a-c ), Fanjul and Barradas ( 1985 ) and Whitehead et al. (1981). These, and studies under controlled environmental conditions (e.g., Pereira and Kozlowski, 1977), generally show stomatal conductance to be strongly influenced by atmospheric humidity deficit and radiation and less strongly by 0168-1923/88/$03.50

© 1988 Elsevier Science Publishers B.V.

leaf' water potential and temperature. However, the responses of differem s p e cies at different seasons may follow a different pattern. For instance, measur~ ments of Beadle et al. t1985b ) in a pine forest show stomatal conductance t~ be quite strongly influenced by vapour pressure deficit, while measurements oi Appleby and Davies {1983) on oak seedlings show little influence ~{ ~apt~',,~ pressure deficit on stomatal behaviour. This paper reports (m measurements of stomatal conductance made m the canopy of an oak forest in The Netherlands. The measurements were used to provide a working model of canopy conductance for use in a P e n m a n - M o n t e i t h type transpiration model. This model and its application to estimate transpiration losses of an oak stand in the Dutch coastal dunes has been described b~ Dolman ( 1988 t. SITE DESCRIPTION ANI) M E A S t R E M E N T S

Forest sit(, The forest is located on the lysimeter site of the Provincial Water Supply Board of North Holland at Castricum (52~33'N, 4 : 3 8 ' E ) . It consists of' oak tree,~ (Quercus robur) planted in 1942. The lysimeter has a total area of 625 m:-'and is 2.5 m deep. At the time the measurements were made, mean tree height war 9.6 m, mean diameter 9.2 cm and stand density 2608 trees ha .2 From mea surements of litter fall later in the year, when leaf ['all was completed, leat are~ index was estimated at 2.0. This rather low value must be attributed ~o ~.~ attack of caterpillars (Tortrix viridana) immediately after leaf emergence. which at t h a t time left little of the canopy. After six weeks a new canopy had been formed. The lysimeters have been filled with sand from the building site from ~he Older Dune sand deposits. Soil development is limited to a slight incorporatiolk of organic material in the first few centimetres of the profile. It can be classified as a typic Quarzipsamment. Measurements of soil-water content t)~ neutron probe indicated t h a t the soil-water d e f c i t was at 12 and at 21% of the max~ mum possible value during the two measurement periods respectively,

Measurement.~ Air temperature and vapour pressure deficit were measured at an i n s t r u m e m height of 10.2 m by platinum resistance thermometers and hair hygrometers. The latter measures relative humidity with an accuracy of 3%. For typical values of temperature in this experiment the corresponding error in vapour pressure d e f c i t will be about 0.05 kPa. Incoming solar radiation was measured by a Kipp C-7 solarimeter at 11.4 m. Leaf conductance was measured with a Delta-T Devices diffusion porometer

101

(Mk II) from a scaffolding tower. The porometer times a 5% rise in relative humidity in a cup clamped to a leaf surface (Stiles, 1970). The Delta-T porometer is calibrated against a polypropylene calibration plate with six known diffusion resistances. The calibration is temperature dependent and should give a linear relationship between resistance and time for a 5% increase in relative humidity. For each temperature, different calibration graphs should be used. Instead of a linear relationship, as recommended by the manufacturer, we used second-order polynomials to describe the relationship between the number of counts and resistance. For each run through the canopy a new calibration curve was made and used for the measurements taken the subsequent hour. Values of conductance were obtained by taking the reciprocal of the resistance as calculated from the calibration graph. All further calculations were performed on conductances. The scaffolding tower was 10 m high and had two wooden platforms of 3 by 1.35 m at 6 and 8 m above the ground. This structure gave access to parts of the canopy of eight trees. Initially, 10 layers each of 50 cm were distinguished but during data processing a division into three layers was found to be sufficient to cover most of the vertical variation in stomatal conductance. One measurement only on the abaxial side of a single leaf was taken to allow for sampling as many different leaves as possible. Oak leaves are known to be hypostomatous; this was confirmed by measurements on the upper side of the leaves that showed conductances of at least one order of magnitude less. In the t o p m o s t two layers, 15 measurements were taken in each layer and in the lowest layer, 20. Layer I comprised leaves from 8.5 m upward, layer II from 7 to 8.5 m and in layer III leaves were sampled from 5 to 7 m. No attempt was made to distinguish between shaded and non-shaded leaves. In about 1 h the complete canopy could be sampled adequately. Measurements were taken from 28 August to 2 September and from 2 to 6 October 1985. RESULTS

Diurnal variation The results are presented first as diurnal plots for selected measurement days. Measurements are presented as the mean value of each layer. Standard errors are typically 5-10% of the mean value. The diurnal variation in stomatal conductance is presented for two days in each measurement period (Fig. 1). Concurrent changes in solar radiation, temperature and vapour pressure deficit are also shown. In general, stomatal conductance is low in the early morning, rises quickly to a maximum value and decreases in the afternoon. The pattern corresponds to patterns commonly found when plotting stomatal conductance against time (Hinckly et al., 1978a; Roberts et al., 1982; Beadle et al., 1985a). On 29 August, stomatal conductance increased rapidly in the morning, stayed

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constant fbr most of the day and decreased in the late afternoon with decreasing solar radiation. On the next day, different behaviour was observed. After a maximum value was reached at 9.00 h for the upper layer, stomatal conduct ance decreased gradually. Behaviour on 5 October was of the same sort as 29 August, but as radiation levels were comparatively low stomatal conductance did not increase as rapidly in the early morning. On 6 October, after 9.00 h, ~ gradual decrease in stomatal conductance was observed. Stomatal conductance decreased with depth in the canopy, although the diJ-

103

ference between the upper and middle layer was less than between the middle and lower layer.

Systematic variation To separate the response of stomatal conductance to the individual environm e n t a l variables, results w e r e g r o u p e d w i t h r e s p e c t t o i n t e r v a l s o f v a p o u r pressure deficit and radiation. Results are shown for the top level only as responses o f t h e t o p layers are t h e clearest. It is n o t e d t h a t t h e l o w e r layers p r e s e n t t h e s a m e t y p e o f r e s p o n s e but w i t h less a m p l i t u d e . M e a s u r e m e n t s f r o m b o t h m e a s u r e m e n t periods are shown.

Figure 2 shows the response of stomatal conductance to incoming solar radiation for vapour pressure deficits below and above 1 kPa. The results suggest an i n c r e a s e up to a v a l u e o f ~ 200 W m - e , t h e r e s p o n s e at v a p o u r p r e s s u r e i •;

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deficits above 1 kPa being less sharp. The response of stomatal conductance to vapour pressure deficit is shown in Fig. ,3 for radiation levels above 20{t W m -2 only. Below this level, radiation seems to be a main limiting factor. Ai higher vapour pressure deficits stomatal conductance has decreased slightly~ It is still around 0.50 cm ~ •~ at: vapour pressure deficits of 2 kPa~ "['be figur~ suggests a low response of stomatal conductance of the oak leaves t~, vapour pressure deficit. No noticable effect of temperature on stomatal conductance could i..,t: discerned. The response of' stomata to individual environmental variables may be described by a model first proposed by Jarvis (1976). This phenomenological model is based on the proposition t h a t essentially all the environmental var~ ables act on the stomata independently, i.e., it assumes a non-synergistic interaction between environment and stomatal aperture. A non-linear o p t i m i zation technique can be used to provide best estimates of the parameters of th~ response functions, which are derived mostly from controlled environment experiments. From the preceding section it may be inferred t h a t ambient vapour pressur~ deficit and solar radiation influence stomatal conductance. A model describim: these influences reads as follows

where g((4~ ) = IQ~/ (a~ +Q~ t lillO0{}/(l.O{}O+a,> }i and g t 6e ) = 1

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where, fie = ambient vapour pressure deficit, Q.~= solar radiation, and a~, a~ an¢~ a~ are parameters found by optimizing eqn. 1 against measured conductances The term [ 1000/( 1000 + a21 ] in eq. 2 serves to normalise g(Q.~ ) to a maximun~ value of one. The value of a~ may be regarded as the maximum possible sl{, matal conductance when no factor is limiting stomatal aperture. The above model was applied to each of the three canopy layers for both measurement periods. The values of the parameters are given in Table 1. Ais,, shown are correlation coefficients and average tractional errors. During both measurement periods the constant az, the maximum stomatai conductance, decreases from the top to the lowest layer. The constant a:~ in the first period is higher for the lower layers, showing a decrease in radiation levels with depth inside the canopy. This effect results from the use of above-canopy radiation data. It is not noticeable in the second period. This may be explained either by the onset of senescence, which may make the stomata less responsiw~ to radiation, or as a result of the use of a restricted variable space, which puts

105 TABLE1 Values of the parameters in t h e stomatal conductance model for the two m e a s u r e m e n t periods Height (m) Leaf area (%) Period a al (cm s - ~) a2 ( k P a - ~) a3 (W m -2) r (obs,est) Mean fractional error N u m b e r of observations

8.5-10.5 48 1 1.057 0.214 104.9 0.65 -0.05 47

2 0.993 0.143 95.8 0.65 -0.05 28

7.0-8.5 33 1 0.964 0.255 153.3 0.60

2 0.9094 0.237 113.6 0.61

5.0-7.0 19 1 0.656 0.216 436.9 0.67

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2 0.5344 0.030 57.8 0.51 -0.08 28

al, m e a s u r e m e n t s from 28 August to 2 September; 2, m e a s u r e m e n t s from 2 to 6 October.

limitations on the use of the optimization technique (e.g., Jarvis, 1976). Especially during the second measurement period, the observed range of radiation and vapour pressure deficit is quite small. Unfortunately, the present data do not allow complete discrimination between the two possibilities, although the data from the first period favour the latter explanation. Except for the lowest layer in the second period, the values of a2, the parameter describing the response to vapour pressure deficit, are of similar magnitude. They show a weak dependence of stomatal conductance on vapour pressure deficit. Correlation coefficients are low, although average fractional errors generally are <10%. DISCUSSION

The behaviour of stomatal conductance in the oak forest of this study is in general agreement with other studies of stomatal conductance in forests or on forest trees, although the absolute values of stomatal conductance are somewhat higher than those reported in the literature (e.g., Holmgrem et al., 1965; Federer, 1976; Hinckley et al., 1978b). These high values may be site specific, as trees located on the lysimeter have free access to an artificially controlled groundwater reservoir and are hardly ever subject to severe water stress. Moreover, at the time of measurement, observed soil-moisture deficits were negligible. It is unlikely that they are a consequence of the fact that the leaves studied here are not primary but regrowth leaves. Turner and Heichel (1977) show that, in the case of oak, two or three weeks after leaf budding, conductances of primary and regrowth leaves are of similar magnitude. Stomatal conductance increases in response to increasing radiation until a saturation level is reached. The response of the lower canopy layers is less sharp. The response to vapour pressure deficit is less pronounced than, for instance, observed in pine trees (Beadle et al., 1985b). Appleby and Davies

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(1983) present a possible explanation tbr this. They suggest that the dif[erent response of stomata of several tree species depends on structural characteris tics of the guard cell complex. In our case the absence of water stress may offer an additional explanation for the low response. The correlation between observations and model predictions is rather poor. It is recognized that the use of above-canopy measurements of radiation and vapour pressure deficit only, will probably result in a substantial amount ol unexplained variance due to the divergence of radiation and vapour pressur¢~ deficit within the canopy. The division into several canopy layers, however, was introduced to remedy this problem. Another source of variation are sam pling errors. Leverenz et al. (1982) analysed sampling errors associated with measurements of stomatal conductance in a pine canopy. They identified several sources of error, several of which do not apply to a deciduous forest. I ) i i ferences in stomatal conductance in a deciduous forest may occur betweeli trees in different positions of dominance, and position of leaves in t:he crowr~ and on a branch. In our case we stratified the canopy and sampled these on several trees randomly. Sampling errors will thus be reflected in the standard errors of the mean values for each layer. As these are generally in the order ot 5-10% of the mean value we conclude that sampling errors are not the most important source of unexplained variance of the model. It should be stressed at this point that the present data clearly show the need for a comprehensiv~ sampling program in which not only top leaves or non-shaded leaves are sam pied. Although this sort of sampling may be illustrative and yield high starts. tical correlations between model predictions and observations, i~ is ,~i considerably less use in canopy conductance or transpiration models in whict~ variation within the canopy is important. The low correlations suggest that factors other than vapour pressure deficil and solar radiation may influence stomatal conductance. We tried to i n c o r porate a possible temperature dependence but this did not result in improved model predictions. A possible clue to the low explanatory power of the model is given in Fig. 4 where fractional errors in stomatal conductance are plotted against time. It can be inferred from this figure that later on in the day model performance decreases quite drastically. A mechanism for this overestimatioi~ of stomatal conductance can be sought in the response of stomatal conduct ance to leaf water potential. Unfortunately this quantity was not measured i~ the present experiment, but it is not unrealistic to assume that as a result of the high radiation levels and vapour pressure deficits encountered during the measurements, transpiration rates during the first part of the day were quite high (estimates by the P e n m a n - M o n t e i t h equation show these to be in excess of 200 W m - ~). This will probably result in a decrease of leaf water p o t e n t i a l which may subsequently reduce stomatal conductance when it falls below e~ certain threshold value. This mechanism has been observed before in d e c i duous forest species (Hinckley et al., 1978a).

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Using the model given above, Dolman (1987) introduced an upper threshold to transpiration on a single day in his model of canopy conductance and transpiration. This zero-order approximation of the effect of leaf water potential on stomatal conductance gave good agreement between measurements of transpiration obtained from the water balance of the lysimeter and model calculations. ACKNOWLEDGEMENTS

The help of H.W. de Groot in collecting porometer data is gratefully acknowledged. Comments by two anonymous referees helped to improve various parts of this paper.

REFERENCES Appleby, R.F. and Davies, W.J., 1983. A possible evaporation site in the guard cell wall and the influence of leaf structure on the humidity response by stomata of woody plants. Oecologia, 56: 30-40. Beadle, C.L., Talbot, H., Neilson, R.F. and Jarvis, P.G., 1985a. Stomatal conductance and photosynthesis in a mature Scots pine forest. I. Diurnal, seasonal and spatial variation in shoots. J. Appl. Ecol., 22: 557-571. Beadle, C.L., Talbot, H., Neilson, R.F. and Jarvis, P.G., 1985b. Stomatal conductance and photosynthesis in a mature Scots pine forest. II. Dependence on environmental variables of single shoots. J. Appl. Ecol., 22: 573-586. Beadle, C.L., Talbot, H., Neilson, R.F. and Jarvis, P.G., 1985c. Stomatal conductance and photosynthesis in a mature Scots pine forest. III. Variation in canopy conductance and canopy photosynthesis. J. Appl. Ecol., 22: 587-595. Beven, K., 1979. A sensitivity analysis of the Penman-Monteith actual evapotranspiration estimates. J. Hydrol., 44: 169-190.

108 Dolman, A.J., 1986. Estimates of roughness length and zero plane displacement for a foliated and a non-foliated oak canopy. Agric. For. Meteorol., 36: 241-248. Dolman, A.J., 1987. Transpiration of an oak forest as predicted from porometer and weather data. J. Hydrol., 97: 225-234. Fanjul, L. and Barradas, V.L., 1985. Stomatal behaviour of two heliophile understorey species of a tropical deciduous forest in Mexico. J. Appl. Ecol., 22: 943-954. Federer, C.A., 1976. Differing diffusive resistance and leaf development may cause differing transpiration among hardwoods in spring. For. Sci., 22: 359-364. Hinckley, T.M., Lassoie, J.P. and Running, S.W., 1978a. Temporal and spatial variations in the water status of forest trees. For. Sci. Mon., 20, 71 pp. Hinckley, T.M., Aslin, R.G., Aubuchon, R.R., Metcalf, C.L. and Roberts, J.E., 1978b. Leaf conductance and photosynthesis in four species of the Oak-Hickory forest type. For. Sci., 24: 7384. Holmgren, P., Jarvis, P.G. and Jarvis, M.S., 1965. Resistances to carbon dioxide and water vapour transfer in leaves of different plant species. Phys. Plant., 18: 556-573. Jarvis, P.G., 1976. The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos. Trans. R. Soc. London B, 273: 593-610. Leverenz, J., Deans, J.D., Ford, E.D., Jarvis, P.G., Milne, R. and Whitehead, D., 1982. Systematic spatial variation of stomatal conductance in a Sitka spruce plantation. J. Appl. Ecol., 19: 835851. Pereira, J.S. and Kozlowski, T.T., 1977. Influence of light intensity, temperature, and leaf area on stomatal aperture and water potential of woody plants. Can. J. For. Res., 7: 145-153. Roberts, J.M., Pitman, R.M. and Wallace, J.S., 1982. A comparison of evaporation from stands of Scots pine and Corsican pine in Thetford Chase, East Anglia. J. Appl. Ecol., 19: 859-872. Stiles, W., 1970. A diffusive resistance porometer for field use. I. construction. J. Appl. Ecol., 7: 617-622. Turner, N.C. and Heichel, G.H., 1977. Stomatal development and seasonal changes in diffusive resistance of primary and regrowth foliage Of red oak (Quercus rubra L. ) and red maple (Acer rubrum L.). New Phytol., 78: 71-81. Whitehead, D., Okali, D.U.U. and Fasehun, F.E., 1981. Stomatal response to environmental variables in two tropical forest species during the dry season in Nigeria. J. Appl. Ecol., 18: 571587.