The Influence of Water Stress and Temperature on Leaf Pubescence Development in Encelia

Farinosa
Author(s): James Ehleringer
Source: American Journal of Botany, Vol. 69, No. 5 (May - Jun., 1982), pp. 670-675
Published by: Botanical Society of America, Inc.
Stable URL: http://www.jstor.org/stable/2442956
Accessed: 10-03-2016 21:30 UTC

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 Amer. J. Bot. 69(5): 670-675. 1982.

THE INFLUENCE OF WATER STRESS AND TEMPERATURE ON

LEAF PUBESCENCE DEVELOPMENT IN ENCELIA FARINOSA1

JAMES EHLERINGER

Department of Biology, University of Utah, Salt Lake City, Utah 84112

ABSTRACT

The degree of leaf pubescence development in the arid land shrub Encelia farinosa Gray is

affected by air temperature, leaf water potential, and previous history of the apical meristem

during the current growing season. Changes in leaf pubescence levels change leaf spectral

characteristics and affect both leaf temperature and photosynthesis. Decreasing leaf water

potentials and increasing air temperatures both independently increase pubescence development

as measured by decreased leaf absorptances. During any one growing season leaf absorptance

may change reversibly coincident with air temperature changes, but with respect to water stress

leaf absorptance only decreases as the season progresses. The ecological significance of reg-

ulation of the leaf spectral characteristics is discussed.

RECENTLY several studies have investigated

low pubescence (high absorptance) because it

the ecological and adaptive aspects of leaf pu-

is possible to reduce leaf temperature via tran-

bescence in desert plants (Ehleringer, Bjork-

spiration. As the soil moisture levels decrease,

man and Mooney, 1976; Smith and Nobel,

transpiration levels decrease and increased leaf

1977; Ehleringer and Bjorkman, 1978a; Ehle-

pubescence is produced (reduced absorp-

ringer and Mooney, 1978; Ehleringer, 1981a).

tance), which again results in a decreased leaf

For the most part, these studies have focused

temperature. A tradeoff occurs because the

on the drought deciduous shrub Encelia fari-

reduced leaf absorptance reduces the rate of

nosa Gray, which seasonally changes the

photosynthesis to an extent proportional to the

amount of pubescence developing on its

decrease in leaf absorptance. However, the

leaves. The changes in leaf pubescence de-

rate of carbon gain by a pubescent leaf is still

velopment cause dramatic changes in leaf spec-

greater than that of a glabrate leaf, because the

tral characteristics, changing the leaf absorp-

decrease in photosynthesis by reflecting quan-

tance (400-700 nm) from 81% under mesic

ta and reducing leaf temperature is less than

periods down to 29% under driest conditions

the decrease in photosynthesis caused by ab-

(Ehleringer and Bjorkman, 1978a). The de-

sorbing those quanta and decreasing photo-

creased leaf absorptance results in lowered leaf

synthesis via increased leaf temperature.

temperatures and rates of water loss (Ehle-

The tight association between pubescence

ringer and Mooney, 1978). Since the photo-

levels, water availability, and air temperature

synthetic apparatus in this species cannot ac-

necessary to result in maximum carbon gain

climate to high temperatures (Ehleringer and

suggests a fine regulation of pubescence de-

Bjorkman, 1978b), the pubescence is an adap-

velopment by the plant. The purposes of this

tive feature allowing the plant to: 1) avoid lethal

study were: 1) to determine the influence of

leaf temperatures; and 2) maintain leaf tem-

naturally varying air temperatures upon the

peratures near levels optimal for photosynthe-

production of leaf pubescence in E. farinosa;

sis (Ehleringer and Mooney, 1978).

2) to determine under controlled temperatures

The adaptive value of leaf pubescence to

in a greenhouse, the effect of desiccation of

Encelia farinosa under moderate and high air

leaf tissue upon induction of leaf pubescence;

temperatures results in a tradeoff, which de-

3) to determine the reversibility of these re-

pends on water availability, but which results

sponses when environmental conditions were

in the highest daily carbon gain for that level

changed; and 4) to provide data on the involve-

of drought (Ehleringer and Mooney, 1978; Eh-

ment of the apical meristem in the induction

leringer, 1980). That is, under high soil mois-

of pubescence.

ture conditions the leaf morphology is one with

MATERIALS AND METHODS-Field studies

of Encelia farinosa were concentrated at two

I Received 12 January 1981; revision accepted 29 May

sites: the Boyd Desert Research Center in

1981.

This study has been supported by NSF Grant No. DEB Deep Canyon, California and at Park Head-

78-10592.

quarters, Death Valley National Monument,

670

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 May-June, 1982] EHLERINGER-PUBESCENCE IN ENCELIA FARINOSA 671

California. Precipitation at both sites falls

E Encelia farinosa

80 - Deep Canyon, Cal.

chiefly during the winter months and averages

92 mm and 42 mm annually for Deep Canyon

o 70

and Death Valley, respectively (U.S. Weather

40

Bureau Records). The performances of watered

o o 60

as well as unwatered shrubs were followed at

each field location. Watered plants received

o 50

Fig. 1.Leafasorptanc not watered

sufficient amounts of water weekly to saturate

and o catered

the soils surrounding the plant (usually about

E 60 -162 f
20-40 1).

Greenhouse studies were conducted in un-

c: 40-

shaded glasshouses during both winter and

Z. 20

summer seasons in which daytime air temper-

atures ranged from 20-25 C. Greenhouse

0 J FM A MJ J ASO N DJ F M AM J J A S 0

plants were grown in 20-1 tubs to reduce pot-

1975 1976

bound effects and, except for experimentally

Fig. 1. Leaf absorptances (400-700 nm) for watered

droughted plants, were watered daily.

and unwatered Encelia farinosa shrubs and precipitation

Changes in leaf pubescence thickness and

data for Deep Canyon, California. Data are means of five

density were quantified by measuring the leaf

samples. Vertical bars represent + 1 standard error.

absorptance to sunlight over 400-700 nm (vis-

ible, photosynthetically useful wavelengths).

Leaf absorptance was measured using a 23-cm

diameter Ulbricht integrating sphere. A he- seasons decreased to as low as 44%. In con-

liostat was used to introduce sunlight into the trast, the leaf absorptances of the watered

integrating sphere. The leaf absorptance is a shrubs varied from 66 to 54% through the sea-

percentage measurement and thus differences son. In response to a record rainfall of 162 mm

in leaf absorptance are differences in the per- (a tropical hurricane) at the end of this exper-

centage of light absorbed by the leaf. Further iment, the absorptances of the watered shrubs

details on the theory and measurement of leaf climbed to 74%. Except for the dramatic

absorptance using this technique are described change at the end of the experiment, the sea-

in Ehleringer and Bjorkman (1978a) and Eh- sonal variation in leaf absorptances of the

leringer (198 lb). watered shrubs was only 12%, compared to a

Leaf water potentials were measured with 41% variation in the leaf absorptances of un-

a Scholander-type pressure chamber. watered plants.

The variations in leaf absorptances of un-

REsULTs-Previous seasonal field observa- watered shrubs followed the rainfall pattern.

tions indicated that the amount of leaf pubes- The highest leaf absorptances were observed

cence produced varied through the course of at the beginning of the growing season, fol-

a growing season, with the greatest variations lowed by a continual decrease through the sea-

occurring in plants at the driest sites (Ehle- son. Immediately following the initial rain-

ringer et al., 1976; Ehleringer and Bjorkman, storm in December there was a rapid flush of

1978a). Since new leaves are formed quickly, larger, green leaves with high absorptances and

the degree of pubescence present on leaves is older leaves were abscised soon after (Fig. 2).

probably a response to recent and/or prevailing Rainfall late in the growing season after the

environmental conditions. Covarying with leaf plants had experienced only mild water stress

pubescence through the season are air tem- (e.g., April, 1975 and May, 1976), did not cause

peratures and leaf water potentials. Given this the plants to develop larger, green leaves with

as the case, how much can the seasonal vari- high absorptances.

ation in pubescence production be reduced by

The seasonal fluctuation in leaf absorptances

watering the plants in the driest sites? of the watered shrubs appeared not to be re-

For this experiment, seasonal fluctuations lated to precipitation patterns. Rather these

in leaf absorptances of five watered shrubs and

leaf absorptances appeared to be negatively

five unwatered shrubs were followed in Deep

related to the seasonal fluctuations in air tem-

Canyon. The leaf absorptances of natural, un- peratures, although the possible interaction of

watered shrubs followed a saw-tooth pattern, water potential in addition to temperature on

similar to previously reported studies (Ehle-

leaf absorptance cannot be ruled out. The leaf

ringer and Bj6rkman, 1978a) (Fig. 1). The

absorptances of the watered shrubs both in

greenest leaves had absorptances as high as Deep Canyon and Death Valley field gardens

85%, while leaf absorptances during the dry were negatively correlated with mean maxi-

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 672 AMERICAN JOURNAL OF BOTANY [Vol. 69

80 I I I

<J_ Encelia forinosa

Encelia forinosa

a watered plants

70 70
80

U~~~~~~~~~~~

0
't f ~~~~~~~~~~~not watered

60 plants

0) watered

> 70 N

I ~~~~~~~~~~~~~N

50

O Deep Canyon, Cal. 4 0

following 65mm rain N

0 20 40 60 80 100

cX

Time, days

X 60 -

Fig. 4. Time course of leaf absorptances (400-700 nm)

o2

for Encelia farinosa leaves in a greenhouse drought ex-

periment. Soils were fully saturated at the beginning of the

< _-* absorptance

experiment. Data are means of five samples. Vertical bars

O-o leaf size represent ? 1 standard error.

50 l l l 0

7654321

Leaf number from tip

mum air temperature (Fig. 3, r2 = 0.76,

Fig. 2. Leaf absorptances (400-700 nm) of individual

P < 0.01).

leaves on an Enceliafarinosa stem following the beginning

In a manner similar to the field watering ex-

of the season rainstorm. Leaves 6-7 were developed be-

periments, several greenhouse experiments

fore the rainstorm, while leaves 1-5 developed after.

were conducted to follow the changes in ab-

sorptance of successively produced leaves of

watered and unwatered E. farinosa shrubs

through time. Unwatered plants started out in

the beginning of the experiment with a fully

charged soil. To produce the green, high ab-

70 sorptance leaves necessary to begin these ex-

Encelia farinosa, watered

periments, the apical meristems of all stems

r 2 0.76

were removed. New green leaves were then

a)

produced from the axillary meristems of the

uppermost leaves. For the first experiment,

Q) S

shrubs were grown from seed collected in Tuc-

0)

son, Arizona (-250 mm precipitation) where

the seasonal fluctuation in leaf absorptance is

approximately 55-82%. In the second drought

experiment, the shrubs were from a population

in Panamint Valley, California (- 100 mm pre-

O 60

cipitation) where the seasonal fluctuation in

leaf absorptance is approximately 40-82%.

In the first greenhouse drought experiment

with ten shrubs, leaf absorptances declined

when water was withheld (Fig. 4). At day 43

of the experiment, the leaf absorptances had

declined from 77% to 63%. The midday leaf

water potentials had fallen from -1.95 MPa to

less than -6.57 MPa. At this time, leaves from

all ten shrubs appeared wilted. On day 44, the

50 l l l
soil for all of the plants was fully charged with

20 30 40 water. For five of the shrubs, water was then

applied daily to keep the soil at field capacity.

Air temperature, ?C

The other five shrubs received no additional

water for the duration of the experiment. Fol-

Fig. 3. Leaf absorptances (400g700 nm) of watered

lowing the addition of the water to the soil, all

Encelia farinosa shrubs in Death Valley and Deep Canyon,

California plotted against mean maximum air temperature. plants put out new leaves which had higher

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 May-June, 1982] EHLERINGER-PUBESCENCE IN ENCELIA FARINOSA 673

80 I I I I '_

Encelia forinosa
a 80

CL

c 70
E

EX
0 ~ ~ ~~ 0

70

O0<

0~~0

0 o0

60

t 60\
o watered

0- not watered

o; 0

plants watered once

50 I I I I

o - Encelia farinoso
0 20 40 60 80 100

r2 =096

Time, days

Fig. 5. Time course of leaf absorptances (400-700 nm)

for watered and unwatered Encelia farinosa shrubs in a

1 40

greenhouse drought experiment. Soils were fully saturated

0 - 1.0 -2.0 -3.0 -4.0

at the beginning of the experiment. Data are means of five

samples. Vertical bars represent + 1 standard error.

Leaf water potential, MPa

Fig. 6. Leaf absorptances (400-700 nm) of Encelia far-

inosa shrubs in the second drought experiment (Fig. 5)

absorptances than were found on the water-

plotted as a function of leaf water potential.

stressed leaves. Leaf water potentials at this

time had increased to -2.56 MPa. The new

leaf absorptances averaged 70%. On day 107, The leaf absorptances of the watered shrubs

62 days after the soil had been charged with remained constant for the 98 day duration of

water, the leaf absorptances of the watered the experiment at approximately 75% (Fig. 5).

shrubs were still 70% and leaf water potentials Leaves from shrubs which did not receive

were -2.13 MPa. The leaf absorptances of the water had absorptances which continually de-

unwatered shrubs had again declined, this time clined from the time of soil moisture saturation.

to 50% and leaf water potentials to less than Leaf absorptances of unwatered shrubs de-

-5.74 MPa. clined from 77% on day 0 to 54% on day 44.

Leaf absorptances of the watered shrubs did These shrubs were watered once on day 45.

not increase above 70%, but instead remained Following this watering, the leaf absorptance

at a constant value, even though the shrubs increased but then followed a continual decline

were well watered daily. This is very similar again. Midday leaf water potentials of the

to the pattern of leaf absorptances seen in the watered shrubs ranged from -1.0 to -1.63

field for watered shrubs. There is no simple MPa, whereas the water potentials of the un-

explanation for the observation that following watered shrubs ranged from -1.07 to -4.07

watering on day 45 the leaf water potential MPa. When the leaf absorptances of droughted

failed to return to its original value of -1.9 and nondroughted shrubs are plotted against

MPa as they were on day 0. It is clear, how- leaf water potentials (Fig. 6), a strong negative

ever, that from day 45 to day 107, both the leaf relationship is observed (r2 = 0.96, P < 0.01).

water potentials and leaf absorptances of the It should be kept in mind though that both leaf

watered shrubs remained essentially constant, water potentials and leaf absorptances were

whereas in the unwatered shrubs both leaf measured on mature leaves. The leaf water

water potentials and leaf absorptances de-

potential inducing a specific pubescence pro-

clined together as they had previously in the duction level during development may be

period from day 0 to day 44. somewhat higher.

In the second drought experiment, plants The results of the greenhouse drought ex-

were divided into two groups. Five shrubs

periments suggest that high leaf absorptances

were watered to maintain the soil at field ca-

can only be obtained if the water potential is

pacity. The other five shrubs were started with

kept high at the time when the meristematic

a fully charged soil, but additional water was

region is first activated. This period of high leaf

withheld until midway through the experiment

absorptances can be maintained by providing

when the soil was again briefly charged with

the shrubs continuously with adequate soil

water. As in the first experiment, the leaf ab-

moisture, thus avoiding any plant water stress.

sorptances were measured at various intervals

However, once the stem has experienced low

during the experiment.

water potentials only leaves with progressively

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 674 AMERICAN JOURNAL OF BOTANY [Vol. 69

greater amounts of pubescence are formed un-

til the meristematic region has undergone se- .40 - Ilndio, California

>15mm during 3 week period

vere drought stress (less than -4.0 MPa) and

is then given adequate moisture. Providing the

.30 -
plant with adequate moisture at a time when

the plant has only experienced a moderate level

of water stress fails to produce leaves of greater

.20

leaf absorptance under both greenhouse and

-Q

field conditions. It is interesting to note that

field plants become drought deciduous at about

.10

-4.0 MPa.

The irreversibility of the relationship be-

tween pubescence development (leaf absorp-

JFMAMJJASOND

tance) and water stress (leaf water potential)

Fig. 7. The probability of receiving 15 mm or more

suggests that some part of the plant is able to

precipitation in a 3-wk period as a function of the time of

detect levels of water stress and to regulate

year in Indio, California. This location is near the Deep

pubescence development depending on the

Canyon study site. Based on data from Gifford, Ashcroft

greatest extent of water stress imposed on the

and Magnuson (1967).

plant. It was hypothesized that the apical mer-

istem exerted a large control over the pubes-

cence development. whereas with constant temperatures (green-

To test this hypothesis, five plants were house conditions), leaf absorptance varied 3 1%

grown in a greenhouse with daily watering (no as water availability (leaf water potentials) de-

water stress, midday q'leaf - 1.6 MPa), al- clined.

lowed to dry out until visibly water stressed At first glance these results are not consis-

(midday qPleaf -4.2 MPa), and then rewa- tent with those of Smith and Nobel (1978) in

tered to field capacity and soil moisture main-

which, under a factorial experimental design,

tained at this level (midday &leaf - 1.7 MPa). leaf pubescence levels (as measured by ab-

At this point, 49 stems from these shrubs were sorptance) in E. farinosa changed very little

chosen and their leaf absorptances were mea-

with water availability (under high light) except

sured; they averaged 69%. The apical meri-

at low temperatures. The Smith and Nobel

stems were removed on approximately half of

study lasted only 25 days. However, if in their

these stems (n = 23), and allowed to remain

study the plants had been partly water stressed

as control on the others (n = 26). Plants were

(when brought in from the field) and now were

watered daily for 30 days and then the ab-

actively growing, then only decreases in tem-

sorptances of the developed leaves on the two

peratures (Fig. 3) and not increases in water

sets of stems were determined. The absorp-

availability (Fig. 6) would result in leaf ab-

tances of the axillary activated meristem leaves

sorptance changes. This arises because par-

now averaged 81% and the control meristem

tially water stressed apical meristems are un-

leaves still averaged 68%. The difference be-

able to once again produce green high

tween the treatment and control was significant

absorptance leaves until they have undergone

(F = 224.7, P < 0.01).

dormancy (Plieaf < -4.0 MPa).

The irreversibility of pubescence develop-

DISCUSSION-This study has demonstrated

ment is clear from field observations (Fig. 1;

that pubescence development in Encelia fari-

also in Ehleringer and Bjorkman, 1978a). Once

nosa changes dramatically through the growing

an active apical meristem has been partially

season and is influenced by current tempera-

stressed, it appears that only leaves with pu-

ture and water stress as well as by previous

bescence levels equal to the "driest" condi-

history of the apical meristem. Shreve (1923),

tions that the plant has been exposed to are

Ehleringer et al. (1976), Smith and Nobel

produced. That the "sensor" for water stress

(1977), and Ehleringer and Bjorkman (1978a)

and "memory" for previous history during the

have shown that pubescence development in-

growing season are perhaps located in the ac-

creased with dry conditions late in the growing

tive apical meristem is suggested by the ex-

season. Our measurements indicate that both

periments with apical meristem removal. The

temperature and leaf water potential influence

advantage to the plant of this lack of revers-

the degree of pubescence development. Under

ibility may be that because high precipitation

more or less constant water availability in the

events late in the growing season are rare. The

field, leaf absorptances of E. farinosa varied

data available indicate that indeed the proba-

12% as temperature changed seasonally;

bility of these late season storms is quite low

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 May-June, 1982] EHLERINGER-PUBESCENCE IN ENCELIA FARINOSA 675

Turner and P. Kramer [eds.], Adaptation of plants to

(Fig. 7). From March to the end of the winter

water and high temperature stress, p. 295-308. John

season (main growing period), the probability

Wiley and Sons, New York.

of receiving a storm that would significantly

. 1981a. Ecology and ecophysiology of leaf pubes-

increase soil moisture conditions is less than

cence in North American desert plants. In E. Rodri-

4%. Given this, maintaining the current pu- guez, P. Healey, and T. Mabry [eds.], Plant tri-

chomes. Plenum Press, New York (in press).

bescent leaf could result in greater net pho-

198 lb. Leaf absorptances of Mohave and Sonoran

tosynthetic gains to the plant than would be

Desert plants. Oecologia 49: 366-370.

expected from excision of the current leaf fol-

, AND 0. BJORKMAN. 1978a. Pubescence and leaf

lowed by production of a less pubescent leaf

spectral characteristics in a desert shrub, Enceliafar-

that may be active for only a brief period of

inosa. Oecologia 36: 151-162.

time. , AND . 1978b. A comparison of photosyn-

thetic characteristics of Encelia species possessing

The mechanisms by which these leaves be-

glabrous and pubescent leaves. Plant Physiol. 62: 185-

come more pubescent under water stress are

190.

presently unknown. The development and

9 , AND H. A. MOONEY. 1976. Leaf pubes-

growth of these linear hairs requires extensive

cence: effects on absorptance and photosynthesis in

cell elongation at a time when a plant is

a desert shrub. Science 192: 376-377.

undergoing stress, a phenomenon which usu- , AND H. A. MOONEY. 1978. Leaf hairs: effects on

physiological activity and adaptive value to a desert

ally results in the cessation of growth activities

shrub. Oecologia 37: 183-200.

(Hsiao, 1973). One component of this process

GIFFORD, R. O., G. L. ASHCROFT, AND M. D. MAGNUSON.

is that elongating hair cells may contain higher

1967. Probability of selected precipitation amounts.

osmotic concentrations than the rest of the

Bulletin T-8. Agricultural Experiment Station, Uni-

leaf, resulting in the higher turgor pressures

versity of Nevada, Reno.

necessary for the extensive cell wall growth.

HSIAO, T. 1973. Plant responses to water stress. Annu.

Rev. Plant Physiol. 24: 519-570.

This study has investigated the means by

SHREVE, E. B. 1923. Seasonal changes in the water re-

which pubescence levels in Encelia farinosa

lations of desert plants. Ecology 4: 266-292.

are regulated. The apical meristem appears to

SMITH, W. K., AND P. S. NOBEL. 1977. Influence of sea-

regulate the extent of pubescence on newly

sonal changes in leaf morphology on water-use-effi-

formed leaves in a manner which is consistent

ciency for three desert broadleaf shrubs. Ecology 58:

with the notion that carbon gain and survival

1033-1043.

, AND . 1978. Influence of irradiation, soil

are maximized.

water potential, and leaf temperature on leaf mor-

phology of a desert broadleaf, Encelia farinosa Gray

LITERATURE CITED

(Compositae). Amer. J. Bot. 65: 429-432.

EHLERINGER, J. 1980. Leaf morphology and reflectance

in relation to water and temperature stress. In N.

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