PHOTOSYNTHESIS IN RELATION TO LEAF ORIENTATION

AND LIGHT INTEROEPTION

By P. E. KRIEDEMAN,* T. F. NEALES,* and D. H. ASHTON*

[Mctnuscript received March 20, 1964]

Summary
This paper examines the photosynthetic response of single attached leaves
(of four different species) to an increasing angle of incidence (8) of incoming radiation.
The intensity of light falling upon a leaf can be deduced from geometrical optics to be
proportional to cos 8. The results reported here suggest that the photosynthetic.
activity of leaves exposed to a limiting light intensity follows a similar relationship.
Explanations of this empirically determined relationship are discussed.

1. INTRODUCTION

The amount of light energy falling upon the foliage of a plant community is
frequently the envi~onmental factor that limits the growth rate of that community
(Donald 1961). Two of the factors that influence the photosynthetic rate of individual
leaves within the canopy, as Verhagen, Wilson, and Britten (1963) have pointed
out, are (i) the disposition of leaves in relation to the incident, light, and (ii) the
optical properties of the leaves themselves. Both of these factors will influence the
proportion of the incident light that is reflected, absorbed, and transmitted. The
optical properties of four types of leaves have been studied experimentally by Tageeva
and Brandt (1961) who indicated that for these studies recourse to the theoretical
principles of geometrical optics is impossible: This is also true if the effect of angle of
incidence (0) of incoming radiation upon individual leaf photosynthetic rate is to be
studied. However, Went (1958) suggested, on the basis of geometrical optics, that
individual leaf photosynthetic rate would be proportional to cos 8;t and that this
emphasized the advantage of large values of 0, such as frequently occur in vertically
disposed foliage, when the incident light intensity was above that required to saturate
the photosynthetic mechanism of a horizontally disposed leaf.
The importance of the angle of incidence of radiation falling on the leaf surfaces
of a foliage has also been thoroughly examined, in a theoretical discussion, by
Warren Wilson (1960).
The present paper describes experiments which examine the relationship
between the angle of incidence of incoming radiation, 0, and the photosynthetic rate
of individual attached leaves of four species. The light intensities used were non~
saturating, and the four leaf types differed in morphology and thickness .
.* Botany School, University of Melbourne, Parkville, Vic.
t It should be noted that Went (1958, p. 233) defined angle of incidence (8') as the angle
between the incoming radiation and the leaf surface. Thus he deduced that the photosynthetic
rate of a leaf would be proportional to sin 8'.

AUBt. J. Biol. Sci., 1964, 17, 591-600

592 P. E. KRIEDEMAN, T. ~. NEALES, AND D. H. ASHTON

II. MATERIAL AND METHODS

The photosynthetic behaviour of single attached leaves v,ras studied for four
different species, viz. Eucalyptus regnans (mountain ash), Beta vulgaris (sugar-beet),
Triticum vulgare (wheat, cv. Sabre), and Glycine max (soybean). Experimental plants
were grown in pots of soil under glasshouse conditions.
Measurements of photosynthesis were conducted in a constant-temperature
room (21 °0) by measuring with an infrared gas analyser the amount of CO 2 absorbed
by an illuminated leaf from a C02-buffered air stream recirculating at 15 litres/min.
The adaxial leaf surface was illuminated with a high-pressure mercury vapour lamp
(HPT 400 W). The lamp's emission oflight was restricted by aluminium foil wrapping
to a narrow zone 5 by 4 em opposite the assimilation chamber. A water~bath,
2·5 em deep and flushed continuously with filtered tap water, was fixed in place
between the lamp and the assimilation chamber to reduce heat transmission. The
Perspex assimilation chamber had internal dimensions 17-5 by 6·5 by 0-8 em and
the experiinental leaf was suspended at the mid-plane of the chamber between two
sets of six fine nichrome wires. These wires ran longitudinally, one'set being suspended
from the lid, and the other set raised above the base of the chamber. This aITangement
enabled a replicable leaf position, and prevented the formation of dead space between
the leaf surface and the wall of the assimilation chamber. In setting up the apparatus,
the lamina was carefully positione.d in the chamber, with its petiole running to the
outside through a groove cut in the end wall. The petiole was then sealed into place
with silicone "rubber" (Silcote 11(4) and while this substance was still setting the
lid of the chamber (with inner edges greased) was clamped in position, rendering
the system gas tight, except for inlet and outlet tubing. The angle of incidence (e)
of incoming radiation could be varied from 0 to 90° by rotating the assimilation
chamber about its longitudinal axis.
The proportion of the incident light transmitted through the Perspex lid (3 mm
thick) of the assimilation chamber was calculated from an empirical determination
of the percentage transmission through the lid (approximately 98%), and by reference
to the reflective properties of Perspex (1.0.1. specifications, undated). The intensity
of illumination at the leaf surface, due to the proportion of light transmitted through
the Perspex, was calculated from the cosine relationship (Lambert's Law). The
relationship between the intensity of illumination on the Perspex and leaf surfaces,
for various values of 8, is given in Figure 1.
During measurements of photosynthesis, the CO 2 concentration of the air in
the assimilation chamber was maintained between certain levels by· adjusting the
input of C02-buffered air into the recirculating system. When, for example, condi-
tions promoted high rates of photosynthesis, the rate of input was increased to
prevent excessive CO 2 depletion, and, conversely, when assimilation rates fell due to
reduced light intensity or lowered e, the input rate was decreased so that the supply
of CO 2 -buffered air would not elevate the CO 2 concentration in the recirculating
system above the prescribed level. During photosynthesis measurements, the mean
CO 2 concentration in the assimilation chamber was maintained at 330 (±20) p.p.m.
except in the experiments on E. regnans where it was kept at 420 (±5) p.p.m.
 PHOTOSYNTHESIS IN RELATION TO LEAF ORIENTATION 593

Differences in the CO 2 concentration of the air entering compared with that of the
air leaving the assimilation chamber were reduced to less than 5 p.p.m. by the fast
rate of recirculation. The leaf's photosynthetic rate usually took about 10 min to
stabilize after an alteration in experimental conditions, and 00 2 assimilation was
measured continuously for a further 10-15 min.
Leaf temperature on the undersurface (away from the light) was measured
with a thermocouple probe (from an Ellab type T.E. 3 electric thermometer) which
entered the assimilation chamber through a stoppered aperture. Leaf temperature
during assimilation measurements never rose above 25°0. Light intensity was
100
I
--- .... -',
'~
PERSPEX SURFACE

''''...
f ,,
LEAF SURFACE
"
·"
>-
<
80
,,
,
w
0 ,,
"<>
•0 '\,
\
"• 60
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~ \
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w \
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>- \
Z \
0

•w
40 \
•>- \
\
\
•zw
0
\
w \
z>- \
<
ii
20 \
< \
• \
\
\
\
I I I I I I I \
0 10 20 '0 40 50 60 70 80 90
ANGLE OF INCIDENCe: OF LIGHT (DEGREES)

Fig. I.-Relative magnitudes of the radiant energy per unit area incident
upon the leaf surface and the lid of the assimilation chamber at different
angles of incidence.

measured within the assimilation chamber, at a position normally occupied by the

leaf, with a selenium photocell (uncorrected to the wavelength response curve of
the human eye) from a Weston lightmeter, model 756. Light intensity readings in
foot-candles were transformed to energy units using the conversion factor from
Gaastra (1959) for the appropriate light source and photocell.
At the end of each experiment, the leaf was detached from the plant, lamina
and petiole were weighed separately, and the lamina was printed on dyeline paper
 594 P. E. KRIEDEMAN, T. F. NEALES, .AND D. H. ASHTON

for area measurement by cutting out and subsequently weighing the print. The
chlorophyll content of the leaf was then determined by macerating the leaf in 80%
acetone and measuring the optical density of a clear extract at 6630 and 6450 A
(in a Unicam spectrophotometer) after the method of MacKinney (1941).

Ill. RESULTS

(a) Structure of the Leaves used for these Experiffnenl8

Some of the physical characteristics of the experimental leaves are given in
Table 1. Plate 1, Figures 1-4, illustrates the anatomy of each type of leaf as seen in

TABLE 1

PHYSICAL CHARACTE~ISTICS OF EXPERIMENTAL LEAVES

Laminar Ratio of
Laminar Chlorophyll
Fresh Area to
Species Area Content
Weight Weight
(sqcm) (mg/sqdm)
(g) (sq em/g)

E. regnans 29·7 0·560 53'0 3·91

B. vulga1'is 40·2 0·945 42'6 4·77

T. vulgat'e 12·6 0·176 71'4 4·69

G, max 50·6 0·531 95'3 1·64

cross-section. These four leaf types represent a considerable range of leaf thickness
and chlorophyll content. The leaf of E. regnaw (Plate 1, Fig. 1) is isobilateral.
Visually, the leaf surfaces of E. regnans and B. vulgaris appeared shiny, whilst those
of T. vulgare and G. max were dull.

TABLE 2

PHOTOSYNTHETIC RATE OF INDIVlDUAL LEAVES OF FOUR SPEOIES

Rate measured at a light intensity of 20 X 10 4 ergs/sec/sq cm

co,
Concentra:t;ion Photosynthetic Rate
Species during
Assimilation
(mg CO,/hr/mg
(mg CO,/hr/leaf) (mg CO,/hr/sq dm)
chlorophyll)
(p.p.m.)

E. regnans 420± 5 8·54 28·75 7·35

B. ,milgaris 330±20 9·25 23·00 4·82

T. vulgare 330±20 2'17 17·25 3·69

G.m= 330±20 5'82 11·50 7·01

 PHOTOSYNTHESIS IN RELATION TO LEAF ORIENTATION 595

(b) Variation of Photosynthetic Rate with Light Intensity, when Light Falls NormaUy
on the Leaf Surface
The response curves relating leaf photosynthetic rate and light intensity for
each of the four types of leaf are given in Figure 2(a). The maximum photosynthetic
rates for each leaf, and the expressions of this on a leaf area, and chlorophyll basis,
are given in Table 2.
100] .. ;::0.:--.... .....::::::--
.................
..............
"'-
"
.' ....•.••:.:~~, ... ~
- - - - E. regnaM

- - - - B. yullari •

- - . - - - T. Yulrare

'b
'~
" •..,...............
.."." .... G.mn

"
BO
"
...... ,\ ,
•••
w
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')\>
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60 \, '
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~

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40 \

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"

•
" 20
\ ...,, '"

t;
z \.\~\
.,
\ \ ,\"
\ \\
o 20 40 60 60
ANGLE OF INCIDENCE OF LIGHT {DEGREES}

Fig. a.-Relative net photosynthesis for single attached leaves of four

species in relation to the incident angle of incoming light.

Light-saturated rates of photosynthesis were attained only with the leaves 0

B. ""/garis and G. max. The maximum rate for the leaf of B. vulgaris (23 mg C0 21
hrlsq dm) was similar to that obtained by Gaastra (1959) for sugar-beet, and was
markedly higher than the value for soybean and wheat leaves (Table 2). However,
when photosynthetic rate was expressed on a chlorophyll basis, the leaf of G. max
(which had the least chlorophyll per unit leaf area-Table 1) was approximately
twice as efficient as the wheat leaf. The photosynthetic activity of E. regnans,
expressed on either a leaf area or chlorophyll basis, was greater than that of the other
three leaves. This superiority may be due to an inherently more efficient structure,
or to the fact that the photosynthesis of this leaf was measured in a gas stream of
greater CO 2 concentration (420 p.p.m.) than was used for the other three leaves
(330 p.p.m.).
596 P. E. KRIEDEMAN, T. F. NEALES, AND D. H. ASHTON

(a) (b)
30 30
E. regrlans E. regnans

20 20 ... ......•.
~ -~.-." ...

'0 '0

0
0 W 20 0 20

B. vulgaris \ B. vulgaris

Ia L 20 ~ 20

-."
I

0
u
1 ,o~
~
I '0

"
W
I

">
Z
~
0 If

"
0
I
0 W 20
0
0 20 40 80 80

"
~ 20r 20
T.vulgare I T.vulgare

'0 10

If ! , 01 " ,!\ '

o 10 20 020406080

G.max G.max

'0 '0

I t , ! or, ',1' ,,\ ,

o 10 20 020406080
10'4 X LIGHT INTENSITY (ERG/SEC/SQ eM) ANGLE OF INCIDENCE OF LIGHT (DEGREES)

Fig. 2.-Net photosynthesis for single attached leaves offour species in relation
to light intensity and the incident angle of incoming light.
 PHOTOSYNTHESIS IN RELATION TO LEAF ORIENTATION 597

(c) Relatirmship between Net Phctosynthetic Rate and the Angle of Incidence of the
Light Falling upon the Leaf Surface
In measuring the effect of alterations in (J on leaf photosynthesis it is necessary
to use a light intensity below saturation level, when (J = 0°, so that there will be no
e
delay in the response of photosynthetic rate to increasing while a limiting light
intensity is being approached. For this reason a constant light intensity of 10 X 10 4
ergs/sec/sq cm was chosen by reference to the photosynthetic response curves already
e
obtained [Fig. 2(a)]. This intensity, when ~ 0', is below the saturation level for all
four types of leaf. For one leaf, that of E. regnans, the response of photosynthesis to
alteration of (} was measured at two additional constant light intensities, namely:
14 X 10 4 and 20 X 10 4 ergs/sec/sq cm. Response curves of similar shape were obtained
for all three light intensities.
The results for all four leaves are plotted in Figure 2(b). The relationship
between the relative rate of net photosynthesis (100% when e ~ 0') and e, for each
of the four leaves, is given in Figure 3. These curves were constructed by replotting
the data from Figure 2(b).
IV. D,SCUSSION

For the purposes of discussion, a simple model of the fate of unidirectional

incident energy (Ei) falling upon a leaf at an angle of incidence (} is given in Figure 4.

E, E,

1
19

I
1/1

Ea LEAF
TISSUE

tE'
Fig. 4.-A simple model of the fate ofradiant energy falling
upon the surface of a leaf at an angle of incidence = (J.

E, is the reflected radiation and Ea and E, the radiation absorbed by and transmitted
through the leaf, respectively. The intensity of radiation at the leaf surface, I, is
equal to E, cos O.
The radiant energy absorbed by the leaf (Ea) can be further apportioned as
follows:
Ea = Erad. + E H20 + E p ,
where Erad . is the energy which heats the leaf and is re-radiated, EH"o the energy
used to vaporize water, and Ep the energy used in photosynthesis.
598 F .. E. KR1EDEMAN, T. F. NEALES, AND D. H. ASHTON

The experimental findings of this paper are summarized in Figure 5 where the
relative mean photosynthetic rate for the four leaves and also the calculated intensity
of illumination at the leaf surface (I), are plotted against cos e.
As may be expected, I is linearly related to cos (); however, this is also true of
the mean photosynthetic rate for values of e ranging from 0 to 80°. Thus, Ea OC I oc
Ei cos (J, and since Ei has been kept constant, Ea is therefore proportional to cos O.
At first sight it appears unlikely that this simple, empirically determined, relationship
would hold over a wide range of values for OJ on account of Fresnel's law of reflection
for unpolarized light from a plane surface. This law demonstrates that for a plane
surface, as () increases from 45 to 80°, so Er increases from approximately 4 to 400/0;
and if Er increases, then the proportional value for Ea. and hence E p , must decrease .

000 '00

... - - -... INCIDENT LIGHT

0----0 NET PHOTOSYNTHESIS

/
~
" '0 '0 "<
1
"om
c
~
"< '0
>
./ "o
J
~
C
o
,
!m
,•
C
m
o, .~
~
"
'.'.
•"
,
'0 ,.• 40 ~
3 ,."
"> , "
~ ,., ,
C
""
,.,
'0 /.~ 20 ~

,.,. ~
"
I I 1 10
o 0-2 0-4 0-6 0-8 1'0
COSINE OF ANGLE OF INCIDENCE OF LIGHT

Fig. 5.-Net photosynthesis (mean for four leaves), and light intensity
at the leaf surface, in relation to the cosine of the angle of incidence
of incoming radiation.

However, the adaxial surface of leaves is not planar and from electron micrographs
of carbon replicas (Plate I, Figs. 5-7), appears exceedingly rough. Therefore
Fresnel's law cannot be validly extended to the present considerations of leaf photo-
synthesis in relation to O. That this is so receives further experimental support from
Tageeva and Brandt (1961) whose measurements of the coefficient of absorption
of white light for three different leaves are given in Table 3 (taken from their Figures
3,4, and 5).
From this table it is evident that Eo does not dinllnish as might be expected
if Er increased according to Fresnel's law. In fact, as 8 increases from 0 to 70°, Er
increases from 7 to only 10% with the Hibiscus leaf, and from 13 to 22% with the
Laduca leaf (Tageeva and Brandt 1961). Hence, for the leaves used in the experiments
 PHOTOSYNTHESIS IN RELATION TO LEAF ORIENTATION 599

reported in the present paper, it seems reasonable to assume that Ea remains approxi-
mately constant as 8 is increased. If Ea does remain constant, then within the
limits of experimental error, it is to be expected that: Ep cc Ea cc I cc El, cos 8, as
is found empirically in Figure 5. Furthermore, the amount of light entering the leaf
decreases as cos B increases and Gaastra (1958) has shown that the efficiency of
light utilization in photosynthesis increases as the intensity of illumination on the
leaf decreases. Thus the slight decrease in Ea which may occur when 8 exceeds 60°

TABLE 3

COEFFICIENT OF ABSORPTION OF WHITE LIGHT BY THE LEAVES OF

HIBISCUS ROSA SINENSIS, LACTUCA SATIVA, AND COLEUS SP. '

Results from Tageeva and Brandt 1961

Coefficient of Absorption (as % of incident light)

Angle of
Incidence
(degrees) H. 1'08a 8inensis L. sativa Coleus sp.

0 89 68 97

30 89 68 97

60 88 67 95

70 86 66 94

(Table 3) is perhaps offset by the absorbed light being used more efficiently in photo-
synthesis. In addition, a re-orientation of the chloroplasts with respect to the direction
of incoming radiation could result in a more complete absorption of light with
increasing angles of 8.
Thus, the photosynthetic rate of a leaf is proportional to the cosine of the
angle of incidence of directional illumination apparently for at least two reasons:
(I) the reflective surface of the leaf does not obey Fresnel's law, and (2) the increase
in photosynthetic efficiency which occurs at low light intensities. This proportionality
was hypothetically proposed by Went (1958) who also considered thepossible adaptive
advantage of leaf arrangements in which 8 is large.

V. ACKNOWLEDGMENTS

We are grateful to Professor J. S. Turner for helpful discussions, and to

Professor F. W. Went, Missouri Botanical Garden, for his criticism of the manuscript.
We are indebted to Dr. T. C. Chambers and the members of the Electron Microscopy
Group of this Department for providing the electron micrographs shown in Plate 1,
Figures 5-7. Mr. E. Matthaei, Microscopy Laboratory, University of Melbourne,
took the photomicrographs shown in Plate I, Figures 1-4, while Mr. R. Muss of this
laboratory constructed the assimilation chamber.
We should also like to thank the Wheat Industry Research Council of Australia
for financial support.
600 P. E. KRIEDEMAN, T. F. NEALES, AND D. H. ASHTON

VI. REFERENOES

DONALD, C. M. (1961).-Competition for light in crops and pastures. In "Mechanisms in Biological

Competition". (Symp. Soc. Exp. BioI. No. 15. pp.282-313.)
GAASTRA, P. (1958).-Light energy conversion in field crops in comparison with the photosynthetic
efficiency under laboratory conditions. Meded. LandhHogesch., Wageningen 58: 1-12.
GAASTRA, P. (1959).-Photosynthesis of crop plants as influenced by light, carhon dioxide,
temperature, and stomatal diffusion resistance. Meded. LandbHogesch., Wageningen 59:
1-68.
1.0.1.
SPECIFICATIONS (undated).-"Perspex" Acrylic Materials. Part 5: Properties. p. 39,
Fig. 14. (Imperial Chemical Industries Ltd., PIa·sties Division, England.)
MACKrNNEY, G. (1941).-Absorption oflight by chlorophyll solutions. J. Biol. Ghem. 140: 315-22.
TAGEEVA, S. V., and BRANDT, A. B. (1961).~Study of optical properties of leaves depending on
the angle of light incidence. In "Progress in Photobiology". pp. 163-9. (Eds. B. C.
Christensen and B. Buchmann.) (Elsevier Publ. Co.: Amsterdam.)
VERHAGEN, A. M. W., WILSON, J. H., and BRITTEN, E. J. (1963).-Plant production in relation to
foliage illumination. Ann. Bot., Lond. (N.S.) 27: 627-40.
WARREN WILSON, J. (1960).-Influence of spatial arrangement offoliage area on light interception
and pasture growth. Proc. 8th Int. Grassl. Congr., Reading, England. pp. 275-9.
WENT, F. W. (1958).-The physiology of photosynthesis in higher plants. Preslia 30: 225-49.
KIUEDElVIAN, NEALES, AND ASH1'ON PLATE 1

PHOTOSYNTHESIS IN RELATION TO LEAl!' ORIENTATION

Figs. 1-4.-Photomicrogl·ftphs of transverse sections of laminal' port,ions fl'om tho fOlll' different
lcaft~'pesused in the experiment.s. x 50. 1, E. regnatls; 2, B. vulgaris; S, ~r. vII/yare; 4, G. ma;l:.

Fig.:l.5-7.-Electron micrographs of carbon replicas of the adaxinl leaf l'iul'fuce (x (250) of

E. l'egnans (iJ), B. mtlgaris (6), and '}'. vulgare (7).

AII81 . .T. Biol. Sci., 1964, 17, 591-600