Plan t and Soil 46, 435-444 (1977) Ms. 2937

V A R I A T I O N S AMONG W O O D Y P L A N T S

IN STOMATAL C O N D U C T A N C E A N D

P H O T O S Y N T H E S I S D U R I N G A N D A F T E R

D R O U G H T *

by W. J. DAVIES** and T. T. KOZLOWSKI

Department of Forestry, University of Wisconsin, Madison, Wisconsin 53706

ABSTRACT

Acer saccharum, Fraxinus americana, Juglans nigra, Acer rubrum, Comus amomum, and Ulmus americana seedlings were subjec ted to a soil d ry ing cycle and then rewatered. A t f requen t in tervals dur ing t i le drying cycle and following rewatering, de te rmina t ions were made of equi l ibr ium photosyn- thesis rates, leaf conductances and leaf water potent ia ls . As the drying cycle progressed, leaf water potent ia ls decreased, s toma ta closed, and rates of t ransp i ra t ion and photosynthes i s were reduced. S t o m a t a of the two Acer species in i t ia l ly were more sensi t ive to wate r stress t h a n were those of the o the r species. At low leaf wa te r potent ia ls , s t oma ta of Juglans and Cornus were more open than those of the o ther species. Photosynthes is of A cer saccha- rum, Frax inus and Juglans was s ignif icant ly reduced by p lan t wa te r stress, while pho tosyn the t i c wa te r use eff iciency of Comus and Juglans was most unfavourable . Photosynthes is / leaf conductance rat ios in wa te r stressed leaves were h igher in Fraxinus t h a n in the o ther species. I m m e d i a t e l y af ter rewater- ing, only l imi ted s toma ta l opening occurred in Acer saccharum and Cornus wi th recovery of s tomata t opening most p ro t r ac t ed in Frax inus and Ulmus. There was ex tended reduct ion of photosynthes is of all species as a result of the soil d ry ing t r ea tment . This effect was most significant in Acer saccharum and Juglans. Surv iva l of p lants on mois t and dry sites is discussed in re la t ion to s toma ta l control of t ransp i ra t ion and metabol ic responses to wate r stress.

INTRODUCTION

Plant water deficits have an overriding regulatory influence on stomatal aperture 25, and in many species systematic relationships

* Research supported by the College of Agricultural and Life Sciences, University of Wisconsin-Madison and the International Shade Tree Conference. The cooperation of the Wisconsin Department of Natural Resources is acknowledged.

** Present address: De~'artment of Biological Sciences, University of Lancaster, Lan- caster, England.

436 W. j . DAVIES AND T. T. KOZLOWSKI

be tween s toma ta l resis tance and leaf wa te r po ten t ia l have been dem- ons t ra t ed 3 s 9 1~ 14 is 271 B a n n i s t e r 1 and others have corre la ted

the leaf wa te r s ta tus at which s t o m a t a close wi th the relat ive

d rought resistance of popula t ions of plants . Ne t photosynthes i s is progress ively reduced b y p lan t wa te r stress,

as a result of s t oma ta l closure and direct effects of desiccation on the pho tosyn the t i c sys t em 23. There are large var ia t ions among species in pho tosyn the t i c response to wa te r stress 26 and W u e n s c h e r and

K o z l o w s k i 2s have re la ted pho tosyn the t i c responses to wa te r

stress and species dis tr ibut ion. Despi te rapid r ehydra t ion of leaves following irr igation, s t o m a t a

of m a n y species c o m m o n l y fail to a t t a in m a x i m u m opening af ter a

period of wa te r stress 20. This ' s t o m a t a l af ter effect ' m a y be associat- ed wi th e levated levels of ABA 26 or CO2 in p lants 19, deficiency of a subs tance which p romotes s t oma ta l opening 16, or slow tu rnove r of

ca rboxy la t ive enzymes 17. Regardless of explanat ion , decreased sto- m a t a l aper tu re bo th during and af ter wa te r stress is advan tageous to

the p lan t in t e rms of wa te r conservat ion. Wi th the above consider- at ions in mind, an exper imen t was designed to de te rmine the effects

of wa te r stress on s t om a t a l responses and photosynthes i s of a range

of woody species dur ing a soil d ry ing cycle and following rewater ing. Species responses were considered in t e rms of p lan t ecology.

METHODS

Potted, three-year-old Acer saccharum Marsh. Fraxinus americana L., and Juglans nigra L., and two-year-old Acer rubrum L., Comus amomum Mill., and Ulmus americana L., seedlings were subjected to a single soil drying cycle and then rewatered. At frequent intervals during the drying cycle and fol- lowing rewatering, estimates were made of equilibrium photosynthesis rates, leaf conductances and leaf water potentials. The plants were stressed to leaf water potentials around --25 bars.

All plants were maintained in a growth chamber under 16 hour days at 12,900 lux (0.15 cal cm -2 rain-l), 25°C day and 20°C night, and 70-90% R.I-I. Twenty four plants of each species were selected for uniformity, and 6 of these plants remained intact and were repeatedly sampled for equilib- rium transpiration and photosynthesis rates. The remaining 18 plants in each set were used to obtain estimates of leaf water potential. I t was considered that the few leaves removed from each plant for this purpose had minimal effect on the soil moisture status in each pot.

Rates of water loss and photosynthesis of the plants were measured in a water-jacketed, plexiglass cuvette (dimensions 10 cm X 10 cm X 25 cm) in an

DROUGHT, STOMATAL CONDUCTANCE, AND PHOTOSYNTHESIS 4 3 7

open s y s t e m s imi la r to t h a t descr ibed b y D a v i e s and K o z 1 o w s k i 14. T ransp i - r a t i o n ra tes were d e t e r m i n e d b y mon i to r ing , w i t h d i f fe ren t ia l t h e r m o c o u p l e p s y c h r o m e t e r s 24, t he changes in w a t e r v a p o u r c o n t e n t of t h e air, before a n d a f t e r i t passed t h r o u g h t h e cuve t te . The rmocoup le s were connec t ed to a W e s t r o n i c s 12-point recorder and, us ing a flow r a t e of 3 l i ters pe r min, a change of 0 .5% in re la t ive h u m i d i t y of t he air could be de tec ted . Ca rbon dioxide exchange was d e t e r m i n e d w i t h a B e c k m a n in f ra - red CO2 ana lyse r in con- j u n c t i o n w i t h a S p e e d o m a x recorder . The recorder scale co r re sponded to 400 ppm, a n d t h e read ings could be i n t e r p o l a t e d to t he nea re s t 1 ppm. The l igh t source was a Luca lox 4 0 0 / B U reversed s p e c t r u m sod ium v a p o u r l amp, pos i t ioned a f ixed d i s t ance f rom the cuve t te . L i g h t i n t e n s i t y and air t e m p e r a t - ure were k e p t c o n s t a n t t h r o u g h o u t t he e x p e r i m e n t a t 24,400 lux, (0.24 cal cm -2 m i n -1) a n d 25°C respect ively . Leaf t e m p e r a t u r e s were m e a s u r e d w i t h t h r ee 0 .003" Cu/Co t h e r m o c o u p l e s a t t a c h e d to t h e lower surface of t h e leaves Air t e m p e r a t u r e s were d e t e r m i n e d w i t h two s imi lar t h e r m o c o u p l e s s i t u a t e d be low t h e leaves. Air e n t e r i n g t h e c u v e t t e was m a i n t a i n e d a r o u n d 70% R.H.

P l a n t s were p laced in t h e c u v e t t e 45 m i n u t e s before m e a s u r e m e n t s were t aken , such t h a t equ i l i b r ium gas exchange ra tes were a t t a i n e d a n d recorded. Gas exchange ra t e s for each p l a n t were ca lcu la ted in m g H 2 0 or CO2/h and expressed b o t h on a leaf a rea bas is a n d in t e r m s re la t ive to ra tes in uns t r e s sed p lan t s . Leaf areas were d e t e r m i n e d b y a p h o t o g r a p h i c pape r -we igh ing t ech- n ique 15. Lea f c o n d u c t a n c e s were ca lcu la ted accord ing to t h e m e t h o d s de- scr ibed b y H o l m g r e n 10. Leaf w a t e r p o t e n t i a l s were d e t e r m i n e d b y t he pres- sure c h a m b e r m e t h o d 2~

RESULTS

As the soil dried, leaf water potentials of all species decreased. Stomatal conductances and net photosynthesis were reduced at lower plant water potentials (higher levels of plant water stress) (Figs. 1 and 2). Stomata ol the two Acer species were most sensitive to leaf water stress, showing abrupt closure at relatively high leaf water potentials. Stomata of Juglans and Cornus remained compara- tively open, even at low water potentials (Fig. I).

As the plants were stressed, photosynthesis was maintained at a significantly higher level in Cornus and the two Acer species than in Fraxinus, Juglans or Ulmus (Fig. 3). Photosynthe~is/stomatal conductance ratios provide some indication of the direct effects of water stress on photosynthesis, i.e. the effects independent of sto- matal closure. Photosynthetic CO2 uptake was most sensitive to water stress in Cornus and Juglans (Table 1), these two species exhibiting low photosynthesis/conductance ratios when the plants

438 W. J. DAVIES AND T. T. KOZLOWSKI

E

cD

C +.J

-O

O

CD

Fig. 1.

• 3~ - - ans

• 3C -

.26

.2;

i A c e r

,

.,,,_ \

A c e r L*, ~ ~ \ rubru ,,,,., "06

- "= ~ " C o r n u s

"°2-1 I - 2 - 6 - 1 0 - 1 4 - 1 8 - 2 2 - 2 4

Plant water potential {bars) S t o m a t a l c o n d u c t a n c e of six species of woody angiosperms, as

inf luenced b y leaf w a t e r po ten t ia l s .

were dried. Fraxinus seedlings exhibited the highest photosynthetic water use efficiency at high water stress.

After rewatering, all species except Juglans regained leaf turgor and, within 24 hours, had leaf water potentials similar to those of non-stressed plants. However, no plant regained full stomatal open- ing or photosynthesis during the experimental period (Figs. 3 and 4). Juglans plants did not recover from drought, exhibiting leaf yellow- ing and general senescence symptoms as soil water became limiting. The recovery of stomatal opening that did occur, took place in Acer

DROUGHT, STOMATAL CONDUCTANCE, AND PHOTOSYNTHESIS 439

Fig. 2.

IOOi

9O

CO

~ 60

~ 50 ~-Cornug

~J ~_ ~ Acer saccharurn

l I 0 1 ~ Ulmus

Fraxinus o I I I " I

- 5 - I0 " 15 "20 -25

Plant water potential (bars) Net photosynthesis of six species of woody angiosperms, as in-

fluenced by leaf water potential.

rubrum, A cer saccharum and Cornus within one day, and in Ulmus and Fraxinus within four days. Recovery of photosynthesis paral- leled increases in transpiration, although photosynthesis rates in Acer saccharum did increase over an extended t ime period. After some limited recovery following rewatering, s tomatal opening and photosynthesis were most severely inhibited in A cer saccharum, while photosynthesis was least inhibited in Comus and Acer rubrum.

DISCUSSION

Under the conditions of this experiment, Juglans nigra seedlings exhibited only limited control over leaf water loss at low leaf water potentials (Fig. 1). In addition, low photosynthet ic water use effi- ciencies (low photosynthesis/leaf conductance ratios) (Table 1)

440

.13

"12

'11

.10

W. J. DAVIES AND T. T. KOZLOWSKI

i Fraxinus

Ulmus

1

~ . 0 9 %

E 0

.07 (3 t -

-06 c I 0

. _ J

-O3 =

.02

Acer rubrum

Cornus

Acer saccharum

Fig. 3.

1 8

Days .after watering

Stomatal conductances of five species of woody angiosperms fol- lowing rewatering after soil drying.

indicated that CO2 exchange of this species was adversely influenced byleaf water stress. A combination of these two characteristics could limit this species to sites where water was readily available.

T o b i e s s e n and K a n a ~7 suggest that stomatal closure at high water potentials, with the consequent decrease in photosynthesis and possible increase in thermal damage to leaves, could put plants

DROUGHT, STOMATAL CONDUCTANCE, AND PHOTOSYNTHESIS 441

m

ID E I00 [ g * T

/ ./1 ~ ' ~ Cornus

"~ Fraxinus -..~ Acer saccharum

.o_o a0 W ~ ~-

Q_

4 N

Days after watering Fig. 4. N e t p h o t o s y n t h e s i s of f ive species of woody ang iospe rms fol lowing

r e w a t e r i n g a f t e r soil dry ing.

TABLE 1

Photosynthesis/leaf conductance ratios of five species of woody angiosperms stressed to a leaf

water potential around --25 bars (mg C02 dm-~h-1/em sec -1)

F r e x i n u s americana 1014

Jug lans nigre 217 Ulmus americana 457 A cer saccharum 300 Cornus a m o m u m 218 A cer r u b r u m 292

at a selective disadvantage on drier sites. Using these criteria, the results of this experiment indicate that the two Acer species might be limited to moist sites. Low photosynthesis/leaf conductance ratios indicated that photosynthetic CO~ fixation in these two spe- cies was unfavourably affected by water stress, further suggesting that these species might compete unsuccessfully on drier sites. C h r i s t e n s e n et al.2 list the two Acer species and Juglans as species adapted to moist sites in northern Wisconsin. In addition to the

442 W. J . DAVIES AND T. T. KOZLOWSKI

sensitivity to water stress demonstrated here, we have shown else- where that stomata of A cer saccharum are quite sensitive to changes in light, humidity, wind and water stress (the latter brought about by leaf excision) 5 6 15.

The high photosynthesis/conductance ratio exhibited by water- stressed Fraxinus americana seedlings indicates a high photosyn- thetic water use efficiency for this species. This characteristic may explain why Fraxinus is often found on dry sites in the boreal and conifer-hardwood forests of the Great Lakes region of the United States 2 7

Following rewatering, it is of some advantage to the plant to limit stomatal opening and thus conserve available water. Maximal sto- matal opening was not obtained in Fraxinus or Ulmus for four days following rewatering. This response suggests that these two species might compete successfully on sites where availability of water was low. Maximal stomatal opening in A cer rubrum and Comus was ob- tained one day after rewatering, while stomata of Acer saccharum showed only very limited recovery from stress-induced closure, de- spite the increased availability of water. Following rewatering, sto- matal conductances equivalent to we-stress values were attained in Fraxinus, Aeer rubrum and Ulmus americana, but not in Acer saccharum or Comus amomum. Stomatal opening was possibly permanently impaired in these species 11, although water stress may have influenced leaf structure and internal tortuosity resistance of the leaf 12. Leaf conductances as expressed in this paper do not dif- ferentiate between stomatal and mesophyll resistances to water loss.

Significantly, the increase in photosynthesis on rewatering fol- lowing drought varied from only about half to nine tenths of the pre- drought values (Fig. 4). Water stress apparently accelerated leaf senescence. This occurred to such an extent in Juglans and Acer saccharum that many plants did not survive.

McCree 18 and D a v i e s 3 have shown that stomatal sensitivity to decreasing leaf water potential may depend on availability of water to the plant during growth. It is therefore important in any controlled environment work that realistic growth conditions should be selected. It is suggested that the situation where a seedling pre- viously well supplied with water is suddenly exposed to an increase in soil moisture stress, is commonly encountered in nature. This

DR OUGHT , STOMATAL C ONDUCTANCE, AND P H O T O S Y N T H E S I S 443

study should therefore provide an indication of the physiological responses of the field grown plant to an increase in plant water stress.

The stomata of the Fraxinus americana seedlings in this s tudy were considerably more sensitive to plant water stress than stomata of seedlings of the same species studied by T o b i e s s e n and K a n a 27. In trying to explain the differences between these results it should be noted that T o b i e s s e n and K a n a used an excised-leaf drying technique to determine stomatal sensitivity to water stress. P a s t e r- n a k and W i l s o n 21 and D a v i e s a have shown that because of rapid drying, the excised leaf drying techniques may tend to under- estimate the water stress sensitivity of stomata, and thus may prove to be unreliable.

In this s tudy we have suggested that species adaptabili ty to a given site may be influenced by several factors. Plants may be limited to moist sites by such diverse physiological characteristics as ex- treme water stress sensitivity of stomata, poor stomatal control of water loss at low water potentials, low photosynthetic water use efficieneies at low water potentials, or poor recovery of leaf gas ex- change following re-watering after drought. Plants showing high photosynthetic water use efficiencies at high levels of water stress and/or delayed stomatal opening following rewatering after drought might compete successfully on drier sites.

Received 15 August 1975. Revised December 1975

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444 DR OUGHT , STOMATAL CONDUCTANCE, AND P H O T O S Y N T H E S I S

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