- Email: [email protected]
Influence of leaf morphology and optical properties on leaf temperature and survival in three mediterranean shrubs
Plant Science Letters, 26 (1982) 47--56 Elsevier Scientific Publishers Ireland Ltd.
47
INFLUENCE OF L E A F MORPHOLOGY AND OPTICAL PROPERTIES ON L E A F TEMPERATURE AND SURVIVAL IN THREE MEDITERRANEAN SHRUBS
I. SZWARCBAUM(SHAVIV)* Faculty of Agriculture, Department of Agricultural Botany, The Hebrew University, Rehovot (Israel) (Received April 23rd, 1981) (Revision received December 4th, 1981 ) {Accepted December 8th, 1981)
SUMMARY Three Mediterranean shrubs, Salvia triloba, Cistus salviifolius and Cistus incanus, which grow side by side in the same habitat and differ in their leaf morphology and behaviour, were compared. The main cause for the differences in the appearance of the leaves lies in the higher light absorption in S. triloba and C. incanus compared with C. salviifolius. The a m o u n t of light absorbed is related to the presence or absence of leaf pubescence. As transpiration cannot overcome the heat load during the summer, alternative mechanisms have evolved in these plants. These mechanisms are: (1) A decrease in surface area through production of smaller leaves; (2) A decrease in surface area by the folding of leaf margins; (3) A difference in leaf properties caused by different hair densities: a sparse cover on the adaxial side and a dense cover on the abaxial surface, coupled with an ability to expose the abaxial side under conditions of water stress.
INTRODUCTION The Mediterranean region in Israel is characterized by its dry h o t summer and high solar radiation. These environmental factors are expected to affect the morphological and physiological adaptation of plants to climatological conditions in various ways. A c o m m o n l y accepted opinion is that plants in arid habitats exhibit leaf pubescence, which reduces light absorption [1,2]. This reduction in light absorption is considered as an adaptive feature of plants growing in arid *Present address: Biochemistry Department, Weizmann Institute of Science, Rehovot 76 100, Israel. 0304--4211/82/0000--0000/$02.75 © 1982 Elsevier Scientific Publishers Ireland Ltd.
48 habitats [2,3]. Measurements of light reflection [4] indicate a greater reflectance in the visible region of the spectrum by species in hot habitats; in tile IR region of the spectrum differences between groups of plants were not so marked, although the greatest reflectance was shown by desert species. The presence of hairs and scales on desert and subalpine plants was correlated with a higher reflectance in the visible, but not necessarily in the IR region of the spectrum. Pubescence also increases the thickness of the air boundary layer along the leaf surface [5] and thereby reduces the rate of water loss. Although Levitt [6] has pointed out that plants are not too successful in avoiding heat and drought stress by means of reducing light absorption, it is of interest that some Mediterranean shrubs grow side by side in the same habitat, but differ in their leaf pubescence and behavior. In order to understand the differences in morphology and appearance, three shrubs, Cistus salviifolius, Cistus incanus and Salvia triloba were chosen for studies of leaf reflection and absorption spectra, leaf temperature in relation to leaf morphology and transpiration rate in relation to air temperature. MATERIALS AND METHODS Measurements of optical properties of the leaves were made at 400-750 nm using an ISCO Spectrophotometer, model SRR. Measurements were taken under field conditions (using a car battery) to avoid the effects of artificial surroundings in the laboratory. A small remote probe on a 3~foot extension was used for measuring spectral energies in small locations. The sensor is equipped with a diffusing screen which acts as a cosine filter. Measurements were taken when the sun was near the zenith. Reflectance was measured by mounting the remote probe on a stand as close as possible to the leaf and in a position to detect maximum reflectance. Transmittance measurements were done by attaching the leaf to the remote probe surface and directing it towards the sun. Scanning electron microscope observations on leaf structure were made with a Jeol, GSM-35C S.E.M. Samples were prepared by fixing pieces of fresh leaves in glutaraldehyde (5% in K÷ phosphate buffer pH 7.2). The fixed leaf tissue was then dried in acetone in four steps increasing 25--100%. The samples were then dried using a CO: critical point drying apparatus, were m o u n t e d on stubs, and gold was evaporated on leaf surface with a sputtering unit (E-500 made by Polaron). Temperature measurements were done with a digital multipoint instrum e n t using a temperature dependent current source (transducer) model AD 590 made by Analog Devices, U.S.A. Sensors were attached to the lower surface of the leaf. Plants of the three tested species were grown in an open area in 6-1 pots for 1 year. Plants were irrigated once a day during the summer and as needed in winter. Transpiration measurements were made on potted plants in a temperature-
49 controlled chamber (Siemens, F.R.G.). Only part of the plant was in the chamber. Light was provided by a p h o t o f l o o d and an arc lamp at 1.6 • 106 erg cm-: s -1 in the center of the chamber. Transpiration was monitored by a Hygrocon humidity sensor (Chem. Res. Corp., U.S.A.). Before each measurement, relative humidity in the chamber was reduced to 20% and the field capacity in the soil was reached by excess watering. Leaf colour was defined according to the Munseff colour charts for plant tissues. RESULTS
(a) Description o f plants and leaves Leaves of C. salviifolius are yellow green (2.5 GY value 6 chroma 8). They are usually flat b u t sometimes tend to bend downwards at the edge (Fig. l(a,b)). These leaves are n o t as pubescent as those of the other t w o species; Fig. 2 (e) demonstrates the upper side o f a C. salviifolius leaf and Fig. 2 (f) the lower side where stomata are located on a ridge structure on the epidermis (Fig. 2(g,h}). The winter leaf of a C. salviifolius plant may reach an area of 16 cm 2 while summer leaves are smaller and reach only 5 cm:. Leaves of C. incanus are green (5.0 GY value 4 chroma 6) and are nearly flat during winter (Fig. 1(c)), b u t soon after the rainy season they fold up in such a way that their abaxial side is bent upwards at an almost right angle (Fig. l ( d ) ) . Leaves of C. incanus are more pubescent than those of C. salviifolius on both sides (Fig. 2(a,d)). The epidermal structure of C. incanus differs from that of C. salviifolius and instead of ridges it has little bumps (Fig. 2(b)). Leaves of Salvia triloba are flat during winter (Fig. l ( e ) ) b u t are markedly bent upwards in summer (Fig. l ( f ) ) so that a large part of the abaxial side faces the sun. The abaxial side is densely pubescent (Fig. 3(b,e)). This causes a difference in colour b e t w e e n the abaxial side (5 GY value 5 chroma 4) and the abaxial side (7.5 GY value 7 chroma 2). Leaf pubescence of S.triloba is denser than in the other t w o species. The pubescence is almost uniform over the leaf surface (Fig. 3(a)) on the upper side and (Fig. 3(e)) on the lower side, and consists of larger trichomes (Fig. 3(d)). These structures differ in their shape from those of the t w o Cistus species (cf. Figs. 2(c) and 2(e)). It should be noted that artificial flattening of the bent leaves of S. triloba during the summer caused their death which was preceded by a definite change in leaf colour. (b ) Optical properties Reflection and transmittance of light for the three species are given in Figs. 4 " 7 . A marked difference was observed between leaf absorption of C. salviifolius and C. incanus, while reflectance was similar. The difference in absorption between the t w o curves of C. salviifolius and C. incanus
50
a m o u n t s t o 0 . 5 5 4 • 102 W m -2. T h u s leaves o f C. incanus a b s o r b m o r e e n e r g y in t h e 4 0 0 - - 7 0 0 n m range o f t h e s p e c t r u m t h a n t h o s e o f C. salviifolius. In S. triloba t h e r e was a m a r k e d d i f f e r e n c e in t h e r e f l e c t a n c e a n d a b s o r p t i o n p r o p e r t i e s o f t h e t w o sides o f t h e leaf. T h e d i f f e r e n c e in r e f l e c t a n c e b e t w e e n t h e adaxial a n d abaxial side is 0 . 7 7 1 • 102 W m -2. T h e d i f f e r e n c e in t r a n s m i t t a n c e b e t w e e n t h e t w o sides o f t h e leaf was 0 . 4 6 0 • 102 W m -2.
Fig. 1. (a,b) C. incanus leaves during winter (a) and summer (b); (c,d) C. salviifolius leaves during winter (c) and summer (d); (e,f) S. triloba leaves during winter (e) and summer (f).
Fig. 2. Scanning electron microscope images of leaves: (a) × 150; (b) x 450; upper side of C. incanus leaf; (e) x 6 0 0 ; enlargement of C. incanus leaf hair; (d) X 150; lower side of • C. i n c a n u s l e a f ; ( e ) × 150 ; upper side of C. salviifolius leaf; (f) × 100; (g) x 240; (h) × 550; lower side of C. salviifolius leaf.
52
Fig. 3. (a) × 10;upper side of S. triloba leaf; (b) × 10;lower side of S. triloba leaf; ic) X 100; scanning electron microscope image of the upper side of S. triloba leaf; (d) × 600; enlargement of S. triloba leaf hair; (e) x 100; scanning electron microscope image of the lower side of S. triloba leaf.
The a m o u n t o f incident solar energy in the wavelength range 400--700 nm was 4 2 0 W • m -2.
(c ) Transpiration measurements No differences in transpiration rate were observed among the three species up to 30°C (Table I), u n d e r field capacity conditions. At higher temperatures t h e transpiration rates o f S . triloba and C. incanus were lower than t h a t of C. salviifolius. (d ) Temperature measurements When leaves o f S. triloba and C. incanus are fully expanded (Table II), indicating there is no shortage o f water, their temperatures are 5--6°C above the air temperature. At the same time the leaf t e m p e r a t u r e o f C. salviifolius remains close to the air temperature. On the ot her hand, when leaf morphology changes by bending, leaf temperatures o f S. triloba and C. incanus were the same as th at o f their surroundings.
53
®
Q 80
8C
60
60
40
40
;~,,/," "
"7 E el
E
~°
/ pl I
20
A
j
-
I
I
400
I
5O0
20
"v'
I
!
600
I
~/,
I
I
400
700
l
i
500
|
i
600
I
700
nm
nm
Fig. 4. T r a n s m i t t e d spectral energy d i s t r i b u t i o n o f light t h r o u g h Cistus leaves: . . . . . C. i n c a n u s ; ~ - ,
,
C. salviifolius.
Fig. 5. R e f l e c t e d spectral energy d i s t r i b u t i o n f r o m Cistus leaves: . . . . .
, C. incanus;
, C. salviifolius.
©
® 8O
80
/'/ / w J
6O
60 "7
E
e-
40
40
/ /
E ~°
°o 20
20
|
400
500
600
700 nm
I
i
400
!
500
|
I
600
i
!
l
700 nm
Fig. 6. T r a n s m i t t e d spectral e n e r g y d i s t r i b u t i o n o f light t h r o u g h S. triloba leaves: - - -~ -, u p p e r side; ~ , l o w e r side. Fig. 7. R e f l e c t e d spectral e n e r g y d i s t r i b u t i o n f r o m S. triloba leaves: - - , . . . . . , l o w e r side.
u p p e r side;
54 TABLE
I
TRANSPIRATION
RATE
IN 10 -6 m g
H : O c m -2 s -~ O F I a O T T E D P L A N T S
a
T e m p . (°C)
C. salviifolius C. incanus S. triloba
20
25
30
35
40
45
1.2 1.5 1.3
3.3 3.1 3.0
4.5 4.2 4.0
6.1 2.2 2.5
5.8 0.7 0.9
3.2 0.2 0.5
a This being the field capacity at various temperatures.
TABLE II LEAF TEMPERATURE MEASURED IN THE FIELD IN MID-AUGUST Air temperature was 35.6°C
C. salviifolius C. incanus S. triloba
Potted plants (expanded leaves)
Natural plants (bent leaves)
At
35.6°C 40.5°C 41.3°C
35.2°C 35.6°C 35.2°C
0.4 4.9 6.1
DISCUSSION
L e a v e s o f C. incanus a b s o r b , in t h e v i s i b l e p a r t o f t h e s p e c t r u m , 1 . 3 cal • s -I • c m -2 m o r e t h a n C. salviifotius. L e t u s d e n o t e t h e e x t r a e n e r g y absorbed by AI. This extra energy must be removed from the leaf, mainly by convection and radiation. Hence we can write: AI=
1.3cal.
s -1 • c m - : =
hcAT+
-
4
EIR a (T~leaf Tsky)
w h e r e h c is t h e c o n v e c t i o n c o e f f i c i e n t = 1 . 2 - 2 . 4 • 1 0 .5 c a l • c m - : • s -1, EIR - - t h e I R e m i t t a n c e = 1.0 a n d o = t h e S t e f a n B o ! t z m a n n c o n s t a n t = 8 . 1 3 . 1 0 -11 c a l . s -1 . c m : Tsky = Tair -- 2 0 ° C Vair = 3 6 ° C A s t h e t e m p e r a t u r e d i f f e r e n c e is s m a l l t h e a b o v e e x p r e s s i o n c a n b e s i m p l i f i e d as f o l l o w s : A I = h c A T + EIR 4 T a o ( T l e a f - Tsky ). A s s u m i n g t h a t t h e t r a n s p i r a t i o n r a t e d o e s n o t c h a n g e , t h e l e a f t e m p e r a t u r e o b t a i n e d is Tair + 9 . 3 ° C . As IR emittance contributes nearly 70% of the heat loss from leaves [7] Tleaf s h o u l d b e i n c r e a s e d b y 6 . 2 ° C a n d w i l l b e a b o v e 4 2 ° C . S h o u l d t h i s p l a n t t r y t o l o s e t h e e x c e s s o f e n e r g y b y e v a p o r a t i v e c o o l i n g , l e a v e s o f C. incanus
55 would have to transpire 1.6 • 10 -6 g H20 • s -~ • cm -2, more than those of C. salviifolius under constant conditions at 27°C. The transpiration rate for most mesophytes with open stomata at Tair = 25°C and R.H. = 50% is 2 10 pg H20 • s -~ • cm -2 [7]. Thus, the excess energy absorbed by C. incanus leaves is equal in magnitude to the energy utilized at a transpiration rate of a typical mesophyte. These numerical estimates indicate that transpiration cannot provide sufficient cooling for C. incanus plants during the summer. Moreover, C. incanus plants in their natural habitat cannot, apparently, tolerate such a high temperature (~40°C) because as can be seen from the results, the transpiration rate decreases even when water is available. We suspect that at this high temperature certain components are damaged and the plant cannot recover. It is clear in this case that theoretically and practically, transpiration cannot remove the excess energy. The obvious way to prevent the heat damage is apparently to diminish the leaf absorbing area, which reduces the difference Tleaf- Tair (see Table II). Thus, the bending changes the leaf morphology by reducing the heat absorption and preventing high leaf temperature. The fact that C. salviifolius leaves are smaller during the summer helps their convective cooling. Such a phenomenon has been predicted and observed by Loomis [8] and Taylor [9]. It was found that as leaf size decreased, convective transfer efficiency increased. Smaller leaves were n o t only cooler but lost more heat per unit leaf area by convection. In S. triloba, leaf morphology differs in winter and in summer and the optical properties of the two sides of the leaf differ as well, as a result of the different density and structure of the epidermal hairs. Since the adaxial side is exposed during the winter, its lower reflectance increases the absorption of photosynthetically active radiation. Soon after the beginning of the dry season, the abaxial side of the leaf, which reflects more light than the adaxial side, is exposed. The same phenomenon was observed by Ehleringer et al. [2] in Encelia species. Ehleringer et al. [10] have also shown in Encelia farinosa that leaf pubescence reduces the absorption of photosynthetically active radiation by 50% compared to the non-pubescent Encelia californica. They indicate that the most highly reflective leaves typically occur during dry summer months. This was combined with higher resistance to water loss. Israeli [ 11 ] and Fritschen [ 12] have shown a decrease in transpiration due to increasing reflectance of leaves in the visible spectrum. Leaves that have a different degree of pubescence on their upper and lower surfaces and which, at the same time, are capable of altering their orientation with respect to the sun in winter and summer, are capable of taking advantage of winter sunshine and of being protected against overheating during the summer. On the other hand, reduction in light absorption during the summer resulted from exposing the dense side of the leaf. This may reduce photosynthesis. However, in the Mediterranean region, light is n o t limiting and, therefore, has no significant effect on productivity [ 13,14]. On the other hand, if leaf temperature is lower, water is conserved and productivity is increased. De Wit [ 15] has constructed a model which indicates that high light intensity and high
56
leaf area index increase the photosynthetic efficiency of the lower leaves, if reflectance increases. This may also be the case for S. triloba plants during the summer. The three species that were examined represent ways by which optical and morphological properties of the leaf can provide drought resistance: (1) by a decrease in light absorption; (2) by a decrease in surface area; (3) by a decrease in surface area combined with increasing reflectance of the abaxial side of the leaf, which enables these plants to photosynthesise whatever conditions prevail. ACKNOWLEDGEMENT
Many thanks are given to Mr. Jan Kallo of the Department of Physics and A s t r o n o m y in Tel-Aviv University, for building the instrument for temperature measurements. This study was supported b y The Fund for the Encouragement of Research-Histadrut, The General Federation of Labour in Israel. REFERENCES 1 D.M. Gates, H.J. Neegan, J.C. Schleter and V.R. Weidner, Appl. Optics, 4 (1965) 11. 2 J. Ehleringer, O. Bjorkman and H.A. Mooney, Science, 192 (1976) 376. 3 H.R. Oppenheimer, Adaptation to drought: Xerophytism, in: Plant-Water Relationships in Arid and Semi-Arid Conditions, Paris, Unesco, 1960. 4 W.D. Billings and R.J. Morris, Am. J. Bot., 38 (1951) 327. 5 J.T. Wooley, Agron. J.,'56 (1964) 569. 6 J. Levitt, Responses of Plants to Environmental Stresses, Academic Press, New York and London, 1972. 7 P.S. Nobel, Biophysical Plant Physiology, W.H. Freeman and Co., San Francisco, 1974, p. 488. 8 W.E. Loomis, Ecology, 46 (1965) 14. 9 S.E. Taylor, Optimal leaf form, in: D.M. Gates and R.B. Schmerl (Eds.), Perspective of Biophysical Ecology, Springer-Verlag, 1975. 10 J. Ehleringer and H.A. Mooney, Oecologia (Berl.), 37 (1978) 183. 11 M. Israeli, The effect of soil surface condition on the energy budget, soil temperature and evaporation rate, Thesis, Fac. Agric. Hebrew Univ. Jerusalem, 1960, p. 76. 12 L.J. Fritschen, Agric. Meteorol., 4 (1967) 55. 13 P. Gaastra, Climatic control of photosynthesis and respiration, in: L.T: Evans (Ed.), Environmental Control of Plant Growth, Academic Press, New York, 1963. 14 J. Bonner, Science, 137 (1962) 11. 15 C.T. De Wit, Centrum Landbouwpubl. Landbouwdocument, 663, 1965, p. 36.
47
INFLUENCE OF L E A F MORPHOLOGY AND OPTICAL PROPERTIES ON L E A F TEMPERATURE AND SURVIVAL IN THREE MEDITERRANEAN SHRUBS
I. SZWARCBAUM(SHAVIV)* Faculty of Agriculture, Department of Agricultural Botany, The Hebrew University, Rehovot (Israel) (Received April 23rd, 1981) (Revision received December 4th, 1981 ) {Accepted December 8th, 1981)
SUMMARY Three Mediterranean shrubs, Salvia triloba, Cistus salviifolius and Cistus incanus, which grow side by side in the same habitat and differ in their leaf morphology and behaviour, were compared. The main cause for the differences in the appearance of the leaves lies in the higher light absorption in S. triloba and C. incanus compared with C. salviifolius. The a m o u n t of light absorbed is related to the presence or absence of leaf pubescence. As transpiration cannot overcome the heat load during the summer, alternative mechanisms have evolved in these plants. These mechanisms are: (1) A decrease in surface area through production of smaller leaves; (2) A decrease in surface area by the folding of leaf margins; (3) A difference in leaf properties caused by different hair densities: a sparse cover on the adaxial side and a dense cover on the abaxial surface, coupled with an ability to expose the abaxial side under conditions of water stress.
INTRODUCTION The Mediterranean region in Israel is characterized by its dry h o t summer and high solar radiation. These environmental factors are expected to affect the morphological and physiological adaptation of plants to climatological conditions in various ways. A c o m m o n l y accepted opinion is that plants in arid habitats exhibit leaf pubescence, which reduces light absorption [1,2]. This reduction in light absorption is considered as an adaptive feature of plants growing in arid *Present address: Biochemistry Department, Weizmann Institute of Science, Rehovot 76 100, Israel. 0304--4211/82/0000--0000/$02.75 © 1982 Elsevier Scientific Publishers Ireland Ltd.
48 habitats [2,3]. Measurements of light reflection [4] indicate a greater reflectance in the visible region of the spectrum by species in hot habitats; in tile IR region of the spectrum differences between groups of plants were not so marked, although the greatest reflectance was shown by desert species. The presence of hairs and scales on desert and subalpine plants was correlated with a higher reflectance in the visible, but not necessarily in the IR region of the spectrum. Pubescence also increases the thickness of the air boundary layer along the leaf surface [5] and thereby reduces the rate of water loss. Although Levitt [6] has pointed out that plants are not too successful in avoiding heat and drought stress by means of reducing light absorption, it is of interest that some Mediterranean shrubs grow side by side in the same habitat, but differ in their leaf pubescence and behavior. In order to understand the differences in morphology and appearance, three shrubs, Cistus salviifolius, Cistus incanus and Salvia triloba were chosen for studies of leaf reflection and absorption spectra, leaf temperature in relation to leaf morphology and transpiration rate in relation to air temperature. MATERIALS AND METHODS Measurements of optical properties of the leaves were made at 400-750 nm using an ISCO Spectrophotometer, model SRR. Measurements were taken under field conditions (using a car battery) to avoid the effects of artificial surroundings in the laboratory. A small remote probe on a 3~foot extension was used for measuring spectral energies in small locations. The sensor is equipped with a diffusing screen which acts as a cosine filter. Measurements were taken when the sun was near the zenith. Reflectance was measured by mounting the remote probe on a stand as close as possible to the leaf and in a position to detect maximum reflectance. Transmittance measurements were done by attaching the leaf to the remote probe surface and directing it towards the sun. Scanning electron microscope observations on leaf structure were made with a Jeol, GSM-35C S.E.M. Samples were prepared by fixing pieces of fresh leaves in glutaraldehyde (5% in K÷ phosphate buffer pH 7.2). The fixed leaf tissue was then dried in acetone in four steps increasing 25--100%. The samples were then dried using a CO: critical point drying apparatus, were m o u n t e d on stubs, and gold was evaporated on leaf surface with a sputtering unit (E-500 made by Polaron). Temperature measurements were done with a digital multipoint instrum e n t using a temperature dependent current source (transducer) model AD 590 made by Analog Devices, U.S.A. Sensors were attached to the lower surface of the leaf. Plants of the three tested species were grown in an open area in 6-1 pots for 1 year. Plants were irrigated once a day during the summer and as needed in winter. Transpiration measurements were made on potted plants in a temperature-
49 controlled chamber (Siemens, F.R.G.). Only part of the plant was in the chamber. Light was provided by a p h o t o f l o o d and an arc lamp at 1.6 • 106 erg cm-: s -1 in the center of the chamber. Transpiration was monitored by a Hygrocon humidity sensor (Chem. Res. Corp., U.S.A.). Before each measurement, relative humidity in the chamber was reduced to 20% and the field capacity in the soil was reached by excess watering. Leaf colour was defined according to the Munseff colour charts for plant tissues. RESULTS
(a) Description o f plants and leaves Leaves of C. salviifolius are yellow green (2.5 GY value 6 chroma 8). They are usually flat b u t sometimes tend to bend downwards at the edge (Fig. l(a,b)). These leaves are n o t as pubescent as those of the other t w o species; Fig. 2 (e) demonstrates the upper side o f a C. salviifolius leaf and Fig. 2 (f) the lower side where stomata are located on a ridge structure on the epidermis (Fig. 2(g,h}). The winter leaf of a C. salviifolius plant may reach an area of 16 cm 2 while summer leaves are smaller and reach only 5 cm:. Leaves of C. incanus are green (5.0 GY value 4 chroma 6) and are nearly flat during winter (Fig. 1(c)), b u t soon after the rainy season they fold up in such a way that their abaxial side is bent upwards at an almost right angle (Fig. l ( d ) ) . Leaves of C. incanus are more pubescent than those of C. salviifolius on both sides (Fig. 2(a,d)). The epidermal structure of C. incanus differs from that of C. salviifolius and instead of ridges it has little bumps (Fig. 2(b)). Leaves of Salvia triloba are flat during winter (Fig. l ( e ) ) b u t are markedly bent upwards in summer (Fig. l ( f ) ) so that a large part of the abaxial side faces the sun. The abaxial side is densely pubescent (Fig. 3(b,e)). This causes a difference in colour b e t w e e n the abaxial side (5 GY value 5 chroma 4) and the abaxial side (7.5 GY value 7 chroma 2). Leaf pubescence of S.triloba is denser than in the other t w o species. The pubescence is almost uniform over the leaf surface (Fig. 3(a)) on the upper side and (Fig. 3(e)) on the lower side, and consists of larger trichomes (Fig. 3(d)). These structures differ in their shape from those of the t w o Cistus species (cf. Figs. 2(c) and 2(e)). It should be noted that artificial flattening of the bent leaves of S. triloba during the summer caused their death which was preceded by a definite change in leaf colour. (b ) Optical properties Reflection and transmittance of light for the three species are given in Figs. 4 " 7 . A marked difference was observed between leaf absorption of C. salviifolius and C. incanus, while reflectance was similar. The difference in absorption between the t w o curves of C. salviifolius and C. incanus
50
a m o u n t s t o 0 . 5 5 4 • 102 W m -2. T h u s leaves o f C. incanus a b s o r b m o r e e n e r g y in t h e 4 0 0 - - 7 0 0 n m range o f t h e s p e c t r u m t h a n t h o s e o f C. salviifolius. In S. triloba t h e r e was a m a r k e d d i f f e r e n c e in t h e r e f l e c t a n c e a n d a b s o r p t i o n p r o p e r t i e s o f t h e t w o sides o f t h e leaf. T h e d i f f e r e n c e in r e f l e c t a n c e b e t w e e n t h e adaxial a n d abaxial side is 0 . 7 7 1 • 102 W m -2. T h e d i f f e r e n c e in t r a n s m i t t a n c e b e t w e e n t h e t w o sides o f t h e leaf was 0 . 4 6 0 • 102 W m -2.
Fig. 1. (a,b) C. incanus leaves during winter (a) and summer (b); (c,d) C. salviifolius leaves during winter (c) and summer (d); (e,f) S. triloba leaves during winter (e) and summer (f).
Fig. 2. Scanning electron microscope images of leaves: (a) × 150; (b) x 450; upper side of C. incanus leaf; (e) x 6 0 0 ; enlargement of C. incanus leaf hair; (d) X 150; lower side of • C. i n c a n u s l e a f ; ( e ) × 150 ; upper side of C. salviifolius leaf; (f) × 100; (g) x 240; (h) × 550; lower side of C. salviifolius leaf.
52
Fig. 3. (a) × 10;upper side of S. triloba leaf; (b) × 10;lower side of S. triloba leaf; ic) X 100; scanning electron microscope image of the upper side of S. triloba leaf; (d) × 600; enlargement of S. triloba leaf hair; (e) x 100; scanning electron microscope image of the lower side of S. triloba leaf.
The a m o u n t o f incident solar energy in the wavelength range 400--700 nm was 4 2 0 W • m -2.
(c ) Transpiration measurements No differences in transpiration rate were observed among the three species up to 30°C (Table I), u n d e r field capacity conditions. At higher temperatures t h e transpiration rates o f S . triloba and C. incanus were lower than t h a t of C. salviifolius. (d ) Temperature measurements When leaves o f S. triloba and C. incanus are fully expanded (Table II), indicating there is no shortage o f water, their temperatures are 5--6°C above the air temperature. At the same time the leaf t e m p e r a t u r e o f C. salviifolius remains close to the air temperature. On the ot her hand, when leaf morphology changes by bending, leaf temperatures o f S. triloba and C. incanus were the same as th at o f their surroundings.
53
®
Q 80
8C
60
60
40
40
;~,,/," "
"7 E el
E
~°
/ pl I
20
A
j
-
I
I
400
I
5O0
20
"v'
I
!
600
I
~/,
I
I
400
700
l
i
500
|
i
600
I
700
nm
nm
Fig. 4. T r a n s m i t t e d spectral energy d i s t r i b u t i o n o f light t h r o u g h Cistus leaves: . . . . . C. i n c a n u s ; ~ - ,
,
C. salviifolius.
Fig. 5. R e f l e c t e d spectral energy d i s t r i b u t i o n f r o m Cistus leaves: . . . . .
, C. incanus;
, C. salviifolius.
©
® 8O
80
/'/ / w J
6O
60 "7
E
e-
40
40
/ /
E ~°
°o 20
20
|
400
500
600
700 nm
I
i
400
!
500
|
I
600
i
!
l
700 nm
Fig. 6. T r a n s m i t t e d spectral e n e r g y d i s t r i b u t i o n o f light t h r o u g h S. triloba leaves: - - -~ -, u p p e r side; ~ , l o w e r side. Fig. 7. R e f l e c t e d spectral e n e r g y d i s t r i b u t i o n f r o m S. triloba leaves: - - , . . . . . , l o w e r side.
u p p e r side;
54 TABLE
I
TRANSPIRATION
RATE
IN 10 -6 m g
H : O c m -2 s -~ O F I a O T T E D P L A N T S
a
T e m p . (°C)
C. salviifolius C. incanus S. triloba
20
25
30
35
40
45
1.2 1.5 1.3
3.3 3.1 3.0
4.5 4.2 4.0
6.1 2.2 2.5
5.8 0.7 0.9
3.2 0.2 0.5
a This being the field capacity at various temperatures.
TABLE II LEAF TEMPERATURE MEASURED IN THE FIELD IN MID-AUGUST Air temperature was 35.6°C
C. salviifolius C. incanus S. triloba
Potted plants (expanded leaves)
Natural plants (bent leaves)
At
35.6°C 40.5°C 41.3°C
35.2°C 35.6°C 35.2°C
0.4 4.9 6.1
DISCUSSION
L e a v e s o f C. incanus a b s o r b , in t h e v i s i b l e p a r t o f t h e s p e c t r u m , 1 . 3 cal • s -I • c m -2 m o r e t h a n C. salviifotius. L e t u s d e n o t e t h e e x t r a e n e r g y absorbed by AI. This extra energy must be removed from the leaf, mainly by convection and radiation. Hence we can write: AI=
1.3cal.
s -1 • c m - : =
hcAT+
-
4
EIR a (T~leaf Tsky)
w h e r e h c is t h e c o n v e c t i o n c o e f f i c i e n t = 1 . 2 - 2 . 4 • 1 0 .5 c a l • c m - : • s -1, EIR - - t h e I R e m i t t a n c e = 1.0 a n d o = t h e S t e f a n B o ! t z m a n n c o n s t a n t = 8 . 1 3 . 1 0 -11 c a l . s -1 . c m : Tsky = Tair -- 2 0 ° C Vair = 3 6 ° C A s t h e t e m p e r a t u r e d i f f e r e n c e is s m a l l t h e a b o v e e x p r e s s i o n c a n b e s i m p l i f i e d as f o l l o w s : A I = h c A T + EIR 4 T a o ( T l e a f - Tsky ). A s s u m i n g t h a t t h e t r a n s p i r a t i o n r a t e d o e s n o t c h a n g e , t h e l e a f t e m p e r a t u r e o b t a i n e d is Tair + 9 . 3 ° C . As IR emittance contributes nearly 70% of the heat loss from leaves [7] Tleaf s h o u l d b e i n c r e a s e d b y 6 . 2 ° C a n d w i l l b e a b o v e 4 2 ° C . S h o u l d t h i s p l a n t t r y t o l o s e t h e e x c e s s o f e n e r g y b y e v a p o r a t i v e c o o l i n g , l e a v e s o f C. incanus
55 would have to transpire 1.6 • 10 -6 g H20 • s -~ • cm -2, more than those of C. salviifolius under constant conditions at 27°C. The transpiration rate for most mesophytes with open stomata at Tair = 25°C and R.H. = 50% is 2 10 pg H20 • s -~ • cm -2 [7]. Thus, the excess energy absorbed by C. incanus leaves is equal in magnitude to the energy utilized at a transpiration rate of a typical mesophyte. These numerical estimates indicate that transpiration cannot provide sufficient cooling for C. incanus plants during the summer. Moreover, C. incanus plants in their natural habitat cannot, apparently, tolerate such a high temperature (~40°C) because as can be seen from the results, the transpiration rate decreases even when water is available. We suspect that at this high temperature certain components are damaged and the plant cannot recover. It is clear in this case that theoretically and practically, transpiration cannot remove the excess energy. The obvious way to prevent the heat damage is apparently to diminish the leaf absorbing area, which reduces the difference Tleaf- Tair (see Table II). Thus, the bending changes the leaf morphology by reducing the heat absorption and preventing high leaf temperature. The fact that C. salviifolius leaves are smaller during the summer helps their convective cooling. Such a phenomenon has been predicted and observed by Loomis [8] and Taylor [9]. It was found that as leaf size decreased, convective transfer efficiency increased. Smaller leaves were n o t only cooler but lost more heat per unit leaf area by convection. In S. triloba, leaf morphology differs in winter and in summer and the optical properties of the two sides of the leaf differ as well, as a result of the different density and structure of the epidermal hairs. Since the adaxial side is exposed during the winter, its lower reflectance increases the absorption of photosynthetically active radiation. Soon after the beginning of the dry season, the abaxial side of the leaf, which reflects more light than the adaxial side, is exposed. The same phenomenon was observed by Ehleringer et al. [2] in Encelia species. Ehleringer et al. [10] have also shown in Encelia farinosa that leaf pubescence reduces the absorption of photosynthetically active radiation by 50% compared to the non-pubescent Encelia californica. They indicate that the most highly reflective leaves typically occur during dry summer months. This was combined with higher resistance to water loss. Israeli [ 11 ] and Fritschen [ 12] have shown a decrease in transpiration due to increasing reflectance of leaves in the visible spectrum. Leaves that have a different degree of pubescence on their upper and lower surfaces and which, at the same time, are capable of altering their orientation with respect to the sun in winter and summer, are capable of taking advantage of winter sunshine and of being protected against overheating during the summer. On the other hand, reduction in light absorption during the summer resulted from exposing the dense side of the leaf. This may reduce photosynthesis. However, in the Mediterranean region, light is n o t limiting and, therefore, has no significant effect on productivity [ 13,14]. On the other hand, if leaf temperature is lower, water is conserved and productivity is increased. De Wit [ 15] has constructed a model which indicates that high light intensity and high
56
leaf area index increase the photosynthetic efficiency of the lower leaves, if reflectance increases. This may also be the case for S. triloba plants during the summer. The three species that were examined represent ways by which optical and morphological properties of the leaf can provide drought resistance: (1) by a decrease in light absorption; (2) by a decrease in surface area; (3) by a decrease in surface area combined with increasing reflectance of the abaxial side of the leaf, which enables these plants to photosynthesise whatever conditions prevail. ACKNOWLEDGEMENT
Many thanks are given to Mr. Jan Kallo of the Department of Physics and A s t r o n o m y in Tel-Aviv University, for building the instrument for temperature measurements. This study was supported b y The Fund for the Encouragement of Research-Histadrut, The General Federation of Labour in Israel. REFERENCES 1 D.M. Gates, H.J. Neegan, J.C. Schleter and V.R. Weidner, Appl. Optics, 4 (1965) 11. 2 J. Ehleringer, O. Bjorkman and H.A. Mooney, Science, 192 (1976) 376. 3 H.R. Oppenheimer, Adaptation to drought: Xerophytism, in: Plant-Water Relationships in Arid and Semi-Arid Conditions, Paris, Unesco, 1960. 4 W.D. Billings and R.J. Morris, Am. J. Bot., 38 (1951) 327. 5 J.T. Wooley, Agron. J.,'56 (1964) 569. 6 J. Levitt, Responses of Plants to Environmental Stresses, Academic Press, New York and London, 1972. 7 P.S. Nobel, Biophysical Plant Physiology, W.H. Freeman and Co., San Francisco, 1974, p. 488. 8 W.E. Loomis, Ecology, 46 (1965) 14. 9 S.E. Taylor, Optimal leaf form, in: D.M. Gates and R.B. Schmerl (Eds.), Perspective of Biophysical Ecology, Springer-Verlag, 1975. 10 J. Ehleringer and H.A. Mooney, Oecologia (Berl.), 37 (1978) 183. 11 M. Israeli, The effect of soil surface condition on the energy budget, soil temperature and evaporation rate, Thesis, Fac. Agric. Hebrew Univ. Jerusalem, 1960, p. 76. 12 L.J. Fritschen, Agric. Meteorol., 4 (1967) 55. 13 P. Gaastra, Climatic control of photosynthesis and respiration, in: L.T: Evans (Ed.), Environmental Control of Plant Growth, Academic Press, New York, 1963. 14 J. Bonner, Science, 137 (1962) 11. 15 C.T. De Wit, Centrum Landbouwpubl. Landbouwdocument, 663, 1965, p. 36.