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Cavitation and resistance to water flow in plant roots
Agricultural Meteorology, 18(1977)21--25
© Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands
CAVITATION AND RESISTANCE TO WATER FLOW IN PLANT ROOTS
G. F. BYRNE, J. E. BEGG* and G. K. HANSEN** Division o f Land Use Research, CSIRO, P. O. B o x 1666, Canberra, A.C.T., 2601 (Australia)
(Received June 1, 1976; accepted December 20, 1976)
ABSTRACT Byrne, G. F., Begg, J. E. and Hansen, G. K., 1977. Cavitation and resistance to water flow in plant roots. Agric. Meteorol., 18:21 25. Large variations in resistance to water flow in plants may be caused by cavitation in root xylem. A relationship is found between resistance to air flow through frozen cotton root segments and stress in the plant from which the segment was taken, thus suggesting a possible method of deducing cavitation and its effect on plant resistance. T h e m e c h a n i s m s b y w h i c h the resistance to the f l o w of w a t e r t h r o u g h plants changes u n d e r field c o n d i t i o n s is basic t o the u n d e r s t a n d i n g o f c r o p g r o w t h a n d t h e d e p l e t i o n o f soil w a t e r and this f a c t has b e e n r e f e r r e d to b y a n u m b e r o f a u t h o r s (e.g., R o s e e t al., 1 9 7 6 ; B y r n e et al., 1976). T h e r e is increasing e v i d e n c e t h a t s u b s t a n t i a l g r a d i e n t s in w a t e r p o t e n t i a l can o c c u r in t h e x y l e m vessels o f p l a n t s (Begg and T u r n e r , 1 9 7 0 ; D e n m e a d a n d Millar, 1 9 7 5 ) , and m e t e o r o l o g i c a l c o n d i t i o n s f a v o u r i n g high e v a p o r a t i v e d e m a n d c a n i n d u c e such g r a d i e n t s even w h e n w a t e r is readily available in the profile. T h e r e is also e v i d e n c e t h a t u n d e r field c o n d i t i o n s leaf w a t e r p o t e n t i a l s in c o t t o n can d r o p to at least - 2 7 0 0 k Pa w i t h o u t a n y sign of s t o m a t a l closure ( J o r d a n a n d Ritchie, 1971). P a t t e r n s o f c h a n g e in s t e m d i a m e t e r w i t h varying w a t e r stress, in which larger changes o c c u r t o w a r d the t o p o f the s t e m and w h i c h display c o n s i d e r a b l e h y s t e r e s i s suggest t h a t s u b s t a n t i a l resistances to axial w a t e r f l o w are p r e s e n t ( K l e p p e r et al., 1971). H o w e v e r , c a l c u l a t i o n s o f Poiseuille resistance to w a t e r f l o w suggest t h a t such resistances are n o t s u f f i c i e n t t o e x p l a i n p o t e n t i a l d r o p s o b s e r v e d in the field. F o r e x a m p l e , D i m o n d ( 1 9 6 6 ) s h o w e d t h a t b y allowing f o r the cond u c t i v i t y o f all x y l e m vessels in t h e t o m a t o p l a n t , o b s e r v e d p r e s s u r e d r o p s c o u l d be s a t i s f a c t o r i l y e x p l a i n e d in t e r m s o f Poiseuille t h e o r y and t h a t t o t a l p r e s s u r e d r o p s were small ( < 1 0 0 k Pa). H o w e v e r , Barrs ( 1 9 7 3 ) has o b s e r v e d p o t e n t i a l s o f - 9 0 0 k Pa in t o m a t o leaves a n d - 1 2 0 0 k Pa in c o t t o n leaves *Present address: Division of Plant Industry, CSIRO, Canberra. ** Present address: Royal Veterinary and Agricultural Laboratory, Copenhagen.
22
of plants with roots m n u t r i e n t solution, when subjected to high evaporatlv ~ demand. One way of reconciling these two apparently c o n t r a d i c t o r y bodies of evi. dence is to a d o p t the hypothesis that., under stress, cavitation (someumes referred to as embolism) occurs and water c o n d u c t i o n ceases in some xyl em vessels. Because of the small dimensions of the xyl em vessels the high pressure in an air a nd/ or vapour " b u b b l e " would result in its dissolving fairly readily once the stress was relieved, thus restoring the integrity of the water co lu mn (Gardner, 1965). Cavitation has been observed in trees (Preston, 1952) and inferred for the petioles of plants (Milburn and Johnson, 1966). The larger x y l e m elements in a section of lateral r o o t from a stressed c o t t o n plant, viewed under reflected light, appear to be e m p t y of water. Five c o t t o n seedlings were grown in a mixture of perlite and vermiculite in pots in a glasshouse with daily watering. They were then subjected to a restricted watering regime which p r o d u c e d a different water stress m each of the plants. Th e fifth and sixth leaves from the top of each plant were excised at the petiole and their water potential was measured using the Scholander b o m b technique (Scholander et N., 1964). At approxi m at el y the same time the plants were carefully removed from the vermiculite, the entire r o o t systems plunged into liquid nitrogen and the intact plants then temporarily stored in plastic bags in a deep freeze unit. Working within the deep freeze unit, one 2 cm section (length 1 :~ 2 cm) of lateral r o o t (diameter ~_ 2 ram) was removed from each plant. One end of the section was c o n n e c t e d to a 10.3 k Pa source (AP) of compressed air and th e other end was placed below the surface of cooled ethyl alcohol and the time t for 0.1 cm ~ of air to flow (q = 0 . 1 / t em 3 s -1 ) through the frozen r o o t was measured using an inverted m i c r o b u r e t t e and stopwatch. Fig.1 ('5 ~
.
.
.
.
.
.
.
.
.
.
.
? ~. 0.3
.
.
.
.
•
0.2 o
0.0 1000
2000
3000
-~lJL (k Pal
Fig.1. Relationship between reciprocal air flow resistance of frozen root sections and plant potential. shows the relationship between the reciprocal of the resistance to air flow (RsA = A P / ( q x 1) k Pa s cm --4) and the mean potential xIJL of the plant, measured as described. It wilt be n o t e d t hat this relationship is linear, suggest
23 ing t h a t the air is flowing through e m p t y (cavitated) xylem vessels and t h a t the extent of cavitation is a function of water stress. That these figures are of the right order, is confirmed by the fact that calculations of Poiseuille air flow resistance using microscope measurements of the xylem vessels of a comparable, but n o t necessarily identical, root section of a cotton plant gave a figure of 270 k Pa s cm -4 (i.e., 1/RsA = 0.37 • 10-2). An important feature of this p h e n o m e n o n is that the largest conducting element would be the first to cavitate and the resulting effect on conductivity would therefore be marked. Using the relationship between the viscosity of air ~/a (170 * 10 -6 P) and that of water ~/co (1 • 10 -2 P), the resistance to water flow in the nowempty xylem vessels RWE may be f o u n d by: RWE = RSA
x
r/co/~ a
RSA
x
58.8
=
(1)
Assuming the xylem elements represent a system of parallel resistances, the total resistance with all vessels water filled, RTOT, is given by: 1 RTOT
1 RWF
1 RWE
Thus, the resistance to water flow of the uncavitated xylem vessels: RWF
-
RTOTRWE R WE -- RTOT
(2)
As shown in Fig.2, with increasing stress RSA shows an asymptotic >10 0 0 0
2500 E u
2000
2 ~5oo 1000
5O0 0 1000
I 2000
3000
I%1 (k Pa)
Fig.2. Relationship between air flow resistance and plant Potential.
24
a p p r o a c h to a value o f a b o u t 200 k Pa s cm -4 indicating an RTO T v a h w ~ll t h e o r d e r o f 200 x 58.8 ,,r 11 700 k Pa s c m --~. T h e f l o w rate in such ,~ lateral r o o t of a c o m p a r a b l e u n s t r e s s e d p l a n t was e s t i m a t e d f r o m the h o u r l y w h o l e - p l a n t transpiratio~l, and a s u b s e q u e n t c o u n t of laterals, t o be 3.({ x 10 -4 c m 3 s-I. Values of RWE can be o b t a i n e d f r o m t h e o b s e r v e d RSA i)v eq. 1. With eq. 2 a n d an e s t i m a t e o f RTOT, the resistance of the t m c a v i t a t e d x y l e m vessels, RWF, can be cah.ulated f r o m these values of RWE. Using the values o f RWF a n d t h e a b o v e e s t i m a t e of the f l o w rate in a lateral (3.~ x 10 -4 c m 3 s -~ ), t h e m a x i m u m p o t e n t i a l d r o p possible A ~ (flux x resistance) in a 1 cm s e g m e n t o f lateral was c a l c u l a t e d ancl p l o t t e d against w a t e r stress as in Fig.3 a s s u m i n g t h e f l o w rate in the lateral to r e m a i n c o n s t a n t .
:
7 E
Q
i I0 L
I000
2000
3000
I~LI (k Pa) Fig.3. E s t i m a t e d r o o t p o t e n t i a l g r a d i e n t p l o t t e d against stress.
T h e r e l a t i o n s h i p suggests t h a t r o o t resistance t o w a t e r f l o w i n c r e a s e d r a p i d l y w h e n w a t e r stress e x c e e d e d - 2 0 0 0 k Pa a n d indicates a highly nonlinear r e l a t i o n s h i p b e t w e e n RWF and - ~ t ' L . R e c e n t e v i d e n c e i n d i c a t i n g a d e c r e a s e in p l a n t r e s i s t a n c e w i t h increasing t r a n s p i r a t i o n (Barrs, 1 9 7 3 ) was o b t a i n e d f o r plants g r o w n in n u t r i e n t s o l u t i o n at levels o f w a t e r stress o f a p p r o x i m a t e l y - 5 0 0 k Pa. While it is t r u e t h a t u n d e r c o n d i t i o n s o f l o w stress, r e s i s t a n c e m a y d e c r e a s e with t r a n s p i r a t i o n , u n d e r severe stress a r a p i d increase in r e s i s t a n c e m a y occur. C a v i t a t i o n in r o o t x y l e m m a y be p a r t l y or w h o l l y r e s p o n s i b l e f o r the l a t t e r p h e n o m e n a . ACKNOWLEDGEMENT
A p p r e c i a t i o n is d u e t o Mr. K. R a t t i g a n f o r t e c h n i c a l assistance.
REFERENCES Barrs, H. D., 1 9 7 3 . C o n t r o l l e d e n v i r o n m e n t studies o f t h e e f f e c t s of variable atmosplm~-ic w a t e r stress o n p h o t o s y n t h e s i s , t r a n s p i r a t i o n a n d w a t e r s t a t u s of Z e a m a y s L a n d o t h e r species. Ecol. Conserv., 5: 2 4 9 - - 2 5 8 .
25 Begg, J. E. and Turner, N. C., 1970. Water potential gradients in field tobacco. Plant Physiol., 46: 343--346. Byrne, G. F., Torssell, B. W. R. and Sastry, P. S. N., 1976. Plant growth curves in mixtures and climatological response. Agric. Meteorol., 16: 37--44. Denmead, O. T. and Millar, B. D., 1975. Water transport in wheat. In: Heat and Mass Transfer in the Biosphere. Wiley, New York, N.Y., p. 395. Dimond, A. E., 1966. Pressure and flow relations in vascular bundles of the tomato plant. Plant Physiol., 41 : 119--131. Gardner, W. R., 1965. Dynamic aspects of soil water availability to plants. Ann. Rev. Plant. Physiol., 16: 323--342. Jordan, W. R., and Ritchie, J. T., 1971. Influence of soil water stress on evaporation, root absorption and internal water status of cotton. Plant Physiol., 48: 783--788. Klepper, B., Douglas, B. and Taylor, H. M., 1971. Stem diameter in relation to plant water stress. Plant Physiol., 48: 683--685. Milburn, H. A. and Johnson, R. P. C., 1966. The conduction of sap, II. Detection of vibrations produced by sap cavitation in R i c i n u s xylem. Planta, 69: 43--52. Preston, R. D., 1952. In: Deformation and Flow in Biological Systems. North Holland, Amsterdam, p. 257. Scholander, P. F., Hammel, H. T., Hemmingsen, E. A. and Bradstreet, E. D., 1964. Hydrostatic pressure and osmotic potential in leaves of mangroves and some other plants. Proc. Nat. Acad. Sci. USA, 52: 119--125. Rose, C. W., Byrne, G. F. and Hansen, G. K., 1976. Water transport from soil through plant to atmosphere: a lumped parameter model. Agric. Meteorol., 16: 171--184.
© Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands
CAVITATION AND RESISTANCE TO WATER FLOW IN PLANT ROOTS
G. F. BYRNE, J. E. BEGG* and G. K. HANSEN** Division o f Land Use Research, CSIRO, P. O. B o x 1666, Canberra, A.C.T., 2601 (Australia)
(Received June 1, 1976; accepted December 20, 1976)
ABSTRACT Byrne, G. F., Begg, J. E. and Hansen, G. K., 1977. Cavitation and resistance to water flow in plant roots. Agric. Meteorol., 18:21 25. Large variations in resistance to water flow in plants may be caused by cavitation in root xylem. A relationship is found between resistance to air flow through frozen cotton root segments and stress in the plant from which the segment was taken, thus suggesting a possible method of deducing cavitation and its effect on plant resistance. T h e m e c h a n i s m s b y w h i c h the resistance to the f l o w of w a t e r t h r o u g h plants changes u n d e r field c o n d i t i o n s is basic t o the u n d e r s t a n d i n g o f c r o p g r o w t h a n d t h e d e p l e t i o n o f soil w a t e r and this f a c t has b e e n r e f e r r e d to b y a n u m b e r o f a u t h o r s (e.g., R o s e e t al., 1 9 7 6 ; B y r n e et al., 1976). T h e r e is increasing e v i d e n c e t h a t s u b s t a n t i a l g r a d i e n t s in w a t e r p o t e n t i a l can o c c u r in t h e x y l e m vessels o f p l a n t s (Begg and T u r n e r , 1 9 7 0 ; D e n m e a d a n d Millar, 1 9 7 5 ) , and m e t e o r o l o g i c a l c o n d i t i o n s f a v o u r i n g high e v a p o r a t i v e d e m a n d c a n i n d u c e such g r a d i e n t s even w h e n w a t e r is readily available in the profile. T h e r e is also e v i d e n c e t h a t u n d e r field c o n d i t i o n s leaf w a t e r p o t e n t i a l s in c o t t o n can d r o p to at least - 2 7 0 0 k Pa w i t h o u t a n y sign of s t o m a t a l closure ( J o r d a n a n d Ritchie, 1971). P a t t e r n s o f c h a n g e in s t e m d i a m e t e r w i t h varying w a t e r stress, in which larger changes o c c u r t o w a r d the t o p o f the s t e m and w h i c h display c o n s i d e r a b l e h y s t e r e s i s suggest t h a t s u b s t a n t i a l resistances to axial w a t e r f l o w are p r e s e n t ( K l e p p e r et al., 1971). H o w e v e r , c a l c u l a t i o n s o f Poiseuille resistance to w a t e r f l o w suggest t h a t such resistances are n o t s u f f i c i e n t t o e x p l a i n p o t e n t i a l d r o p s o b s e r v e d in the field. F o r e x a m p l e , D i m o n d ( 1 9 6 6 ) s h o w e d t h a t b y allowing f o r the cond u c t i v i t y o f all x y l e m vessels in t h e t o m a t o p l a n t , o b s e r v e d p r e s s u r e d r o p s c o u l d be s a t i s f a c t o r i l y e x p l a i n e d in t e r m s o f Poiseuille t h e o r y and t h a t t o t a l p r e s s u r e d r o p s were small ( < 1 0 0 k Pa). H o w e v e r , Barrs ( 1 9 7 3 ) has o b s e r v e d p o t e n t i a l s o f - 9 0 0 k Pa in t o m a t o leaves a n d - 1 2 0 0 k Pa in c o t t o n leaves *Present address: Division of Plant Industry, CSIRO, Canberra. ** Present address: Royal Veterinary and Agricultural Laboratory, Copenhagen.
22
of plants with roots m n u t r i e n t solution, when subjected to high evaporatlv ~ demand. One way of reconciling these two apparently c o n t r a d i c t o r y bodies of evi. dence is to a d o p t the hypothesis that., under stress, cavitation (someumes referred to as embolism) occurs and water c o n d u c t i o n ceases in some xyl em vessels. Because of the small dimensions of the xyl em vessels the high pressure in an air a nd/ or vapour " b u b b l e " would result in its dissolving fairly readily once the stress was relieved, thus restoring the integrity of the water co lu mn (Gardner, 1965). Cavitation has been observed in trees (Preston, 1952) and inferred for the petioles of plants (Milburn and Johnson, 1966). The larger x y l e m elements in a section of lateral r o o t from a stressed c o t t o n plant, viewed under reflected light, appear to be e m p t y of water. Five c o t t o n seedlings were grown in a mixture of perlite and vermiculite in pots in a glasshouse with daily watering. They were then subjected to a restricted watering regime which p r o d u c e d a different water stress m each of the plants. Th e fifth and sixth leaves from the top of each plant were excised at the petiole and their water potential was measured using the Scholander b o m b technique (Scholander et N., 1964). At approxi m at el y the same time the plants were carefully removed from the vermiculite, the entire r o o t systems plunged into liquid nitrogen and the intact plants then temporarily stored in plastic bags in a deep freeze unit. Working within the deep freeze unit, one 2 cm section (length 1 :~ 2 cm) of lateral r o o t (diameter ~_ 2 ram) was removed from each plant. One end of the section was c o n n e c t e d to a 10.3 k Pa source (AP) of compressed air and th e other end was placed below the surface of cooled ethyl alcohol and the time t for 0.1 cm ~ of air to flow (q = 0 . 1 / t em 3 s -1 ) through the frozen r o o t was measured using an inverted m i c r o b u r e t t e and stopwatch. Fig.1 ('5 ~
.
.
.
.
.
.
.
.
.
.
.
? ~. 0.3
.
.
.
.
•
0.2 o
0.0 1000
2000
3000
-~lJL (k Pal
Fig.1. Relationship between reciprocal air flow resistance of frozen root sections and plant potential. shows the relationship between the reciprocal of the resistance to air flow (RsA = A P / ( q x 1) k Pa s cm --4) and the mean potential xIJL of the plant, measured as described. It wilt be n o t e d t hat this relationship is linear, suggest
23 ing t h a t the air is flowing through e m p t y (cavitated) xylem vessels and t h a t the extent of cavitation is a function of water stress. That these figures are of the right order, is confirmed by the fact that calculations of Poiseuille air flow resistance using microscope measurements of the xylem vessels of a comparable, but n o t necessarily identical, root section of a cotton plant gave a figure of 270 k Pa s cm -4 (i.e., 1/RsA = 0.37 • 10-2). An important feature of this p h e n o m e n o n is that the largest conducting element would be the first to cavitate and the resulting effect on conductivity would therefore be marked. Using the relationship between the viscosity of air ~/a (170 * 10 -6 P) and that of water ~/co (1 • 10 -2 P), the resistance to water flow in the nowempty xylem vessels RWE may be f o u n d by: RWE = RSA
x
r/co/~ a
RSA
x
58.8
=
(1)
Assuming the xylem elements represent a system of parallel resistances, the total resistance with all vessels water filled, RTOT, is given by: 1 RTOT
1 RWF
1 RWE
Thus, the resistance to water flow of the uncavitated xylem vessels: RWF
-
RTOTRWE R WE -- RTOT
(2)
As shown in Fig.2, with increasing stress RSA shows an asymptotic >10 0 0 0
2500 E u
2000
2 ~5oo 1000
5O0 0 1000
I 2000
3000
I%1 (k Pa)
Fig.2. Relationship between air flow resistance and plant Potential.
24
a p p r o a c h to a value o f a b o u t 200 k Pa s cm -4 indicating an RTO T v a h w ~ll t h e o r d e r o f 200 x 58.8 ,,r 11 700 k Pa s c m --~. T h e f l o w rate in such ,~ lateral r o o t of a c o m p a r a b l e u n s t r e s s e d p l a n t was e s t i m a t e d f r o m the h o u r l y w h o l e - p l a n t transpiratio~l, and a s u b s e q u e n t c o u n t of laterals, t o be 3.({ x 10 -4 c m 3 s-I. Values of RWE can be o b t a i n e d f r o m t h e o b s e r v e d RSA i)v eq. 1. With eq. 2 a n d an e s t i m a t e o f RTOT, the resistance of the t m c a v i t a t e d x y l e m vessels, RWF, can be cah.ulated f r o m these values of RWE. Using the values o f RWF a n d t h e a b o v e e s t i m a t e of the f l o w rate in a lateral (3.~ x 10 -4 c m 3 s -~ ), t h e m a x i m u m p o t e n t i a l d r o p possible A ~ (flux x resistance) in a 1 cm s e g m e n t o f lateral was c a l c u l a t e d ancl p l o t t e d against w a t e r stress as in Fig.3 a s s u m i n g t h e f l o w rate in the lateral to r e m a i n c o n s t a n t .
:
7 E
Q
i I0 L
I000
2000
3000
I~LI (k Pa) Fig.3. E s t i m a t e d r o o t p o t e n t i a l g r a d i e n t p l o t t e d against stress.
T h e r e l a t i o n s h i p suggests t h a t r o o t resistance t o w a t e r f l o w i n c r e a s e d r a p i d l y w h e n w a t e r stress e x c e e d e d - 2 0 0 0 k Pa a n d indicates a highly nonlinear r e l a t i o n s h i p b e t w e e n RWF and - ~ t ' L . R e c e n t e v i d e n c e i n d i c a t i n g a d e c r e a s e in p l a n t r e s i s t a n c e w i t h increasing t r a n s p i r a t i o n (Barrs, 1 9 7 3 ) was o b t a i n e d f o r plants g r o w n in n u t r i e n t s o l u t i o n at levels o f w a t e r stress o f a p p r o x i m a t e l y - 5 0 0 k Pa. While it is t r u e t h a t u n d e r c o n d i t i o n s o f l o w stress, r e s i s t a n c e m a y d e c r e a s e with t r a n s p i r a t i o n , u n d e r severe stress a r a p i d increase in r e s i s t a n c e m a y occur. C a v i t a t i o n in r o o t x y l e m m a y be p a r t l y or w h o l l y r e s p o n s i b l e f o r the l a t t e r p h e n o m e n a . ACKNOWLEDGEMENT
A p p r e c i a t i o n is d u e t o Mr. K. R a t t i g a n f o r t e c h n i c a l assistance.
REFERENCES Barrs, H. D., 1 9 7 3 . C o n t r o l l e d e n v i r o n m e n t studies o f t h e e f f e c t s of variable atmosplm~-ic w a t e r stress o n p h o t o s y n t h e s i s , t r a n s p i r a t i o n a n d w a t e r s t a t u s of Z e a m a y s L a n d o t h e r species. Ecol. Conserv., 5: 2 4 9 - - 2 5 8 .
25 Begg, J. E. and Turner, N. C., 1970. Water potential gradients in field tobacco. Plant Physiol., 46: 343--346. Byrne, G. F., Torssell, B. W. R. and Sastry, P. S. N., 1976. Plant growth curves in mixtures and climatological response. Agric. Meteorol., 16: 37--44. Denmead, O. T. and Millar, B. D., 1975. Water transport in wheat. In: Heat and Mass Transfer in the Biosphere. Wiley, New York, N.Y., p. 395. Dimond, A. E., 1966. Pressure and flow relations in vascular bundles of the tomato plant. Plant Physiol., 41 : 119--131. Gardner, W. R., 1965. Dynamic aspects of soil water availability to plants. Ann. Rev. Plant. Physiol., 16: 323--342. Jordan, W. R., and Ritchie, J. T., 1971. Influence of soil water stress on evaporation, root absorption and internal water status of cotton. Plant Physiol., 48: 783--788. Klepper, B., Douglas, B. and Taylor, H. M., 1971. Stem diameter in relation to plant water stress. Plant Physiol., 48: 683--685. Milburn, H. A. and Johnson, R. P. C., 1966. The conduction of sap, II. Detection of vibrations produced by sap cavitation in R i c i n u s xylem. Planta, 69: 43--52. Preston, R. D., 1952. In: Deformation and Flow in Biological Systems. North Holland, Amsterdam, p. 257. Scholander, P. F., Hammel, H. T., Hemmingsen, E. A. and Bradstreet, E. D., 1964. Hydrostatic pressure and osmotic potential in leaves of mangroves and some other plants. Proc. Nat. Acad. Sci. USA, 52: 119--125. Rose, C. W., Byrne, G. F. and Hansen, G. K., 1976. Water transport from soil through plant to atmosphere: a lumped parameter model. Agric. Meteorol., 16: 171--184.