AOBPreview originally published online on December 7, 2004
Annals of Botany 2005 95(3):483-494; doi:10.1093/aob/mci047
Annals of Botany 95/3 © Annals of Botany Company 2004; all rights reserved
Development of the Monsi–Saeki Theory on Canopy Structure and Function
TADAKI HIROSE*
Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan
* E-mail hirose{at}mail.tains.tohoku.ac.jp
Received: 30 June 2003
Returned for revision: 7 October 2003
Accepted: 12 March 2004
Published electronically: 7 December 2004
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ABSTRACT
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• Background and Aims Monsi and Saeki (1953)
published the first mathematical model of canopy photosynthesis that was based on the light attenuation within a canopy and a light response of leaf photosynthesis. This paper reviews the evolution and development of their theory.
• Scope Monsi and Saeki showed that under full light conditions, canopy photosynthesis is maximized at a high leaf area index (LAI, total leaf area per unit ground area) with vertically inclined leaves, while under low light conditions, it is at a low LAI with horizontal leaves. They suggested that actual plants develop a stand structure to maximize canopy photosynthesis. Combination of the Monsi–Saeki model with the cost–benefit hypothesis in resource use led to a new canopy photosynthesis model, where leaf nitrogen distribution and associated photosynthetic capacity were taken into account. The gradient of leaf nitrogen in a canopy was shown to be a direct response to the gradient of light. This response enables plants to use light and nitrogen efficiently, two resources whose supply is limited in the natural environment.
• Conclusion The canopy photosynthesis model stimulated studies to scale-up from chloroplast biochemistry to canopy carbon gain and to analyse the resource-use strategy of species and individuals growing at different light and nitrogen availabilities. Canopy photosynthesis models are useful to analyse the size structure of populations in plant communities and to predict the structure and function of future terrestrial ecosystems.
Key words:
Monsi–Saeki theory, Boysen Jensen, canopy photosynthesis, light, nitrogen, resource use, cost–benefit analysis, competition, coexistence, size structure, model, plant community
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INTRODUCTION
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Masami Monsi (1914–1997) and Toshiro Saeki (1927–2004)
published the paper ‘Über den Lichtfaktor in den
Pflanzengesellschaften und seine Bedeutung für die Stoffproduktion’
(‘On the factor light in plant communities and its importance
for matter production’) in the
Japanese Journal of Botany in 1953. This paper is now well known as the first that presented
a mathematical model of canopy photosynthesis. They quantified
attenuation of light through the canopy and modelled canopy
photosynthesis as an integration of photosynthesis of leaves
exposed to different light climates in the canopy. They demonstrated
that stand structures develop to maximise canopy photosynthesis
under a given light climate. The paper opened a new research
area on canopy structure and function and is still an inspiration
for plant ecologists, botanists and agronomists today. Yet,
in spite of its importance, its acceptance by scientists in
the western hemisphere was delayed by more than ten years (de
Wit, 1965
; Monteith, 1965
; Ross, 1981
; for review see Monsi
et al., 1973
), probably because it was published in German in
a local journal.
There is a history behind the development of any new idea, and the Monsi–Saeki theory is no exception. It has its roots in the work of Boysen Jensen (1932), a Danish plant physiologist. Boysen Jensen (1883–1959) was the founder of the science of dry mass production of plants. He wrote in the preface of his book (1932) that ‘sie bilden einen Versuch, den Schwerpunkt der Lehre von der Stoffproduktion der Pflanzen dorhin zu verlegen, wo sie meiner Meinung nach liegen muß: In die CO2-Assimilation der Blätter’ (‘those publications attempt to shift the emphasis of the study of biomass production by plants to where, according to me, it should be: leaf CO2 assimilation’). He thus emphasized CO2 assimilation of leaves in the study of dry mass production in plants. He first studied canopy photosynthesis in relation to stand structure, and suggested the importance of leaf arrangement in the plant stand. Suppose a stand has a LAI (leaf area index, total leaf area per unit ground area) of 3, i.e. the stand maintains a leaf area three times more than the ground area beneath it. When leaves are arranged horizontally as shown in Fig. 1A(a), only leaves in the first layer receive full light, whereas leaves in lower layers receive light that has penetrated the first layer and that is close to or less than the light compensation point. If the same amount of leaf area is arranged with inclinations within the canopy [Fig. 1A(b)], then light reaches every leaf more uniformly. Boysen Jensen noted that actual plants indeed have canopies with vertically inclined rather than horizontal leaves to distribute light uniformly within the canopy and thus to use light efficiently. For another example, Boysen Jensen established a small experimental stand of plants to measure the whole-canopy photosynthesis of the stand. He demonstrated that canopy photosynthesis was not saturated, while photosynthesis of a single leaf was saturated at relatively low light intensities (Fig. 1B).
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THE MONSI–SAEKI THEORY OF CANOPY PHOTOSYNTHESIS
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Monsi and Saeki (1953)
refined the idea of Boysen Jensen to
develop a quantitative theory of canopy structure and function.
They devised a stratified clipping technique to describe the
structure of plant communities. Vertical distribution of plant
mass was presented in a figure separately for photosynthetic
and non-photosynthetic tissues together with a distribution
of light intensity (see
fig. 1 in Monsi and Saeki, 1953
; reproduced
in this issue). This figure was named ‘the productive
structure of a plant community’ to imply that plant function
is determined by the structure of the stand and, inversely,
that the stand structure is determined by plant functions. Light
attenuates more strongly in a stand of plants having horizontal
leaves (broad-leaf type) than in a stand with vertical leaves
(grass type). They found that light attenuation in the canopy
was approximated by Beer's Law:
 | (1) |
where
I is the photosynthetic photon flux density (PPFD) measured
on a horizontal plane,
F is the leaf area index cumulated from
top of the canopy, and
K is the extinction coefficient.
I0 is
the PPFD above the canopy. They showed that if small horizontal
leaves were distributed randomly in the canopy,
K should be
equal to 1. In reality, leaves are not small enough to comply
with theory and are sometimes large, they are not horizontal
but inclined, and they are not randomly distributed but are
clumped or uniformly distributed.
K-values deviate from 1 accordingly,
and change from 0·3 to 2·0 (Monsi and Saeki, 1953
).
They noted that
K in a canopy with horizontal leaves was commonly
0·7–1·0, whereas
K in a canopy with vertically
inclined leaves was 0·3–0·5.
The PPFD that leaves receive within the canopy (I') is different from PPFD on a horizontal plane (I) because leaves are not horizontally distributed in the canopy. They showed that I' is calculated from eqn (1) as
 | (2) |
where
m is the
transmittance of a leaf (Saeki, 1960
). It is assumed that only
leaves intercept PPFD in the canopy. A rectangular hyperbola
was employed to describe the net photosynthesis of a single
leaf (
p) as a function of
I':
 | (3) |
where
a and
b are constants that characterise the light-response curve,
and
r is dark respiration (Tamiya, 1951
). Substituting
eqn (2) into
(3) and integrating with respect to
F from 0 to
F, they
calculated canopy photosynthesis,
P, as
 | (4) |
(Monsi and Saeki, 1953
; Saeki, 1960
). This equation was tested
with the
Sinapis alba stand of Boysen Jensen assuming
m = 0
and
K = 1, and with the parameters for leaf photosynthesis of
this species (
Fig. 1B). The result (table 8a in Monsi and Saeki,
1953
) gave a good agreement with the experimental result, as
is shown by the open circles here in
Fig. 1B.
Equation 4 implies
that canopy photosynthesis is determined by stand structure
(
K and
F), leaf physiology (
a,
b and
r), an optical property
of a leaf (
m), and the light environment (
I0).
Figure 2A shows canopy photosynthesis under full light conditions as a function of F. Canopy photosynthesis of the stand is maximized with a low K at a higher F. This result demonstrates well why many canopies developing under full sunlight have a value of K around 0·7 and LAI around 5. The optimal LAI is defined by the lowest leaves that receive PPFD at the light compensation point (I'c), where daily leaf photosynthesis is cancelled out by respiration. At the light compensation point, the following two equations hold:
 | (5) |
and
 | (6) |
Eliminating
I'
c from both equations, the optimal
LAI (
Fopt) was derived:
 | (7) |
Substitution
of
eqn (7) for
F in
(4) gives the maximal canopy photosynthesis
[
Pmax =
P(
Fopt)]:
 | (8) |
This
Pmax is
plotted against the relative incident radiation for different
K-values in
Fig. 2B, which shows that a canopy with a small
K responds to irradiance more strongly than one with a large
K. At high irradiance canopy photosynthesis is maximized at
a small
K, whilst at low irradiance it is maximized at a larger
K. These predictions are in agreement with our every-day experience:
thick vegetation develops in open habitats, where most leaves
are vertically inclined. In forest understoreys, we see flat
leaves sparsely distributed in one layer. Kuroiwa (1971)
proposed
an ideal distribution of leaf angles in the canopy in which
leaves change their angle from vertical at the top to horizontal
at the bottom. However, many species in open habitats have leaf
angles more horizontal than the expectation from the optimization
theory. Later, Hikosaka and Hirose (1997)
showed that in an
evolutionary stable pattern of leaf angles of individuals subject
to competition, the leaves are more horizontal than would lead
to maximal photosynthesis. In the period of the International
Biological Programme (IBP, 1964–1974), the Monsi–Saeki
theory was broadly applied to study primary production in a
range of plant communities from grasslands to forests and from
natural vegetation to agricultural crops (Monsi, 1968
; Monsi
et al., 1973
; Kira, 1975
; Saeki, 1975
).
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FIG. 2. (A) Daily canopy photosynthesis of a Celosia cristata stand under full daylight (100 %) calculated from eqn (4), plotted as a function of leaf area index. Different K-values are assumed. (B) Daily maximum canopy photosynthesis as a function of relative incident radiation. Calculated from eqn (8) for different K-values. Redrawn after Saeki (1960).
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The canopy photosynthesis model of Monsi and Saeki (1953)
explained
well the different stand structures that develop depending on
a given light environment. However, some caveats should be stated
here. First, the assumption that every leaf in the canopy has
the same photosynthetic characteristics is not true. Sun and
shade leaves differentiate within a stand and they have different
photosynthetic capacities from each other (Boardman, 1977
; Björkman,
1981
). [McCree and Troughton (1966)
suggested that the optimal
LAI as assumed by Monsi and Saeki (1953)
would not exist because
shade leaves have a lower light compensation point.] However,
Saeki (1959)
noted that as the contribution of shaded leaves
to total canopy photosynthesis was small, canopy photosynthesis
calculated based on the photosynthesis of sun leaves gave virtually
the same result as that calculated based on different photosynthetic
capacities between sun and shade leaves. As will become clear
from the remainder of this review, consideration of the photosynthetic
capacity of leaves in different layers in the canopy provides
new insights into canopy photosynthesis with respect to the
resource use strategy of plants. The second caveat to be noted
is that Monsi and Saeki (1953)
assumed diffuse light (or overcast
conditions, with parallel light coming from all directions)
to derive
eqn (1), on which their canopy photosynthesis model
was built. Under sunny conditions, however, light distribution
is more heterogenous within the canopy: deep in the canopy,
some leaves that receive sunflecks are sun-lit, whilst the others
are shaded to different degrees. In such a situation, an assumption
of overcast conditions over-estimates canopy photosynthesis,
owing to the non-linearity of the light response of photosynthesis.
The role of diffuse vs direct light on canopy photosynthesis
was considered first by de Wit (1965)
and Duncan
et al. (1967)
,
and has received renewed interest by Gu
et al. (1999)
and Roderick
et al. (2001) (see Farquhar
et al., in later issue)
. The third
caveat is that however well the ‘optimal’ LAI might
explain the natural pattern observed, it must not be interpreted
that the optimum has been realized at the stand level through
natural selection. Individuals, not whole stands of vegetation,
are the unit of natural selection (Williams, 1966
). The optimal
may be realized in isolated individuals and in those that produce
a large canopy, such as clonal plants and trees, but not in
individuals interacting and competing with each other (see Anten,
2005
). Nonetheless, the theory and the concept of optimal LAI
has a practical importance for agricultural management and the
breeding of cultivars to increase crop yields (Loomis and Williams,
1969
).
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COST–BENEFIT ANALYSIS OF RESOURCE USE
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Mooney and Gulmon (1979)
introduced the concept of costs and
benefits in the study of resource use by plants with an econometric
analogy. It is well known that there is a strong correlation
between photosynthetic capacity and leaf nitrogen (Natr, 1975
;
Field and Mooney, 1986
), because more than half of the nitrogen
in a leaf is directly involved in photosynthesis (Evans, 1989
;
Evans and Seemann, 1989
). The rate of photosynthesis increases
with increasing protein content of a leaf. A question then arises:
why don't all plants have high leaf-protein contents and hence
high photosynthetic rates? Mooney and Gulmon (1979)
answered
this question by assuming costs in manufacturing proteins for
photosynthetic carbon gains. In a light-limited habitat, photosynthesis
saturates at a lower enzyme content than in a light-unlimited
habitat (
Fig. 3), indicating that plants growing in low light
conditions should have leaves with low enzyme contents. Now
assume that there are costs (
C) in manufacturing enzyme proteins
(
E) and that the costs increase with increasing investment of
proteins. To maximize net carbon gain [i.e. the difference between
photosynthesis (
P) and
C,
P –
C], the partial derivative
of (
P –
C) with respect to
E should equal to zero:
(
P –
C)/
E = 0. Then,
 | (9) |
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FIG. 3. Photosynthesis (P) increases with increasing enzyme content (E), but saturates at higher E. Saturation starts earlier in a light-limited (A) than light-unlimited (B) habitat. The slope of the tangent lines represents the cost (C) of manufacturing one unit of enzyme. The tangent point defines the optimal enzyme investment (EA,opt and EB,opt) that maximizes photosynthesis per enzyme content. See text for further explanation. Modified from Mooney and Gulmon (1979).
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This equation defines the optimal amount of enzymes that should
be invested within a leaf. The left- and right-hand sides of
this equation are called ‘marginal gain’ and ‘marginal
cost’, respectively. While marginal gain decreases with
an increase in enzyme investment, plants should invest to the
point at which the marginal cost (represented by the tangent
lines in
Fig. 3) exceeds the marginal gain. Note that the optimal
enzyme content is smaller in a light-limited than in a light-unlimited
habitat (
Fig. 3).
Field (1983) formulated the allocation of leaf nitrogen for the maximization of carbon gain as
 | (10) |
where
pday is the daily carbon gain,
nL is leaf nitrogen per
unit leaf area and
is a constant. This equation may be derived
from
eqn (9) by substituting
P and
C for
pday and
nL, respectively,
with the assumption that the marginal cost is constant. Since
at high
nL the marginal gain is higher at high rather than at
low irradiance, nitrogen should be allocated in the canopy such
that leaves receiving the highest irradiance have the highest
nitrogen per unit leaf area. Field (1983)
applied this concept
to a Californian chaparral shrub
Lepechinia calycina and calculated
daily carbon gain for different distributions of nitrogen in
the canopy. However, profits from distributing nitrogen non-uniformly
in the canopy were not large. The optimal distribution increased
canopy photosynthesis by 3 % and the actual distribution increased
it by 1 %, as compared with uniform distribution. Field suggested
that 1–3 % benefits can be still larger than the cost
involved in nitrogen redistribution (i.e. protein degradation,
transport and loading of amino acids, and re-synthesis of proteins).
Mooney
et al. (1981)
demonstrated that nitrogen redistribution
is much more rapid in annual species native to closed-canopy
habitats than in annuals of open habitats, implying that the
potential importance of nitrogen distribution in the canopy
increases with a larger gradient of irradiance. Assuming that
photosynthetic capacity is linearly related to leaf nitrogen,
Charles-Edwards
et al. (1987)
described a pattern of
nL that
declines in proportion to the degree of shade within a canopy.
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LEAF NITROGEN DISTRIBUTION AND CANOPY PHOTOSYNTHESIS
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Hirose and Werger (1987
a,
b)
studied canopy photosynthesis in
a
Solidago altissima stand. This is a clonal species that produces
many leaves along a tall stem without branching, and often makes
a dense, pure stand in flood plains and in an abandoned fields
(Iwaki
et al., 1969
; Hirose, 1971
; Kitamoto, 1972
). Hirose and
Werger (1987
b)
found that leaf nitrogen content per area (
nL)
decreased exponentially with increasing LAI cumulated from the
top of the canopy (
F):
 | (11) |
where
Ft is the total LAI,
n0 is leaf nitrogen per area at the top
of the canopy, and
Ka is the coefficient of nitrogen allocation
in the canopy.
Ka = 0 indicates a uniform distribution of nitrogen,
in which every leaf has a nitrogen concentration equal to the
mean.
Ka increases with increasing non-uniformity of nitrogen
distribution where upper leaves have higher nitrogen per unit
leaf area than lower ones.
Hirose and Werger (1987b) modelled canopy photosynthesis of the Solidago stand, extending the Monsi–Saeki model with nitrogen distribution in the canopy being taken into account. Leaf net photosynthesis (p) as a function of PPFD (I') was described by a non-rectangular hyperbolic equation (Johnson and Thornley, 1984):
 | (12) |
This equation includes
four parameters:
, the initial slope;
pmax, the light-saturated
rate of photosynthesis;
, a curvature factor; and
r, dark respiration.
As these parameters were found to be a function of leaf nitrogen
per area (
nL), leaf net photosynthesis was calculated for a
given leaf nitrogen under a given irradiance (Hirose and Werger,
1987
a). Combining light [
eqn (2)] and nitrogen [
eqn (11)] distribution
within the canopy and leaf photosynthesis as a function of light
and nitrogen [
eqn (12)] with a daily change in PPFD gave a daily
canopy carbon gain.
Table 1 shows the effect of nitrogen distribution on daily canopy carbon gain. A large increase was found in actual and optimal nitrogen distribution as compared with uniform distribution. Non-uniform distribution benefited actual plants by 21 %, although the value was lower than the 27 % increase assumed by an optimal distribution. Large profits of non-uniform nitrogen distribution were demonstrated both in herbaceous species, Lysimachia vulgaris (27 % increase in actual over uniform distribution, Pons et al., 1990) and Carex acutiformis (28 %; Werger and Hirose, 1991; Schieving et al., 1992a), and in a broad-leaved evergreen tree Nothofagus fusca (6 %, Hollinger, 1996). Anten et al. (1995a) showed that profits from non-uniform distribution in actual plants were larger in dicots (41 % in Glycine max and 35 % in Amaranthus cruentus) than in monocots (14 % in Oryza stativa and 13 % in Sorghum bicolor). However, none of these plants attained the optimal N distribution. Actual plants distribute N more uniformly than the optimal distribution. Why didn't plants exhibit optimal N-distribution when this optimization would further enhance their carbon gain? A clue may be found in the range of nitrogen concentrations (see the last column in Table 1). The difference between actual and optimal distribution implies that optimal nitrogen distribution leads to leaf nitrogen per unit area that is too low at the bottom and too high at the top to be realized. Some nitrogen may not be capable of translocation, and a certain amount of nitrogen is necessary to utilize sunflecks that leaves receive in lower layers in the canopy (see Pons et al., 1990). On the other hand, high nitrogen may be risky: when plants are subjected to herbivory, they would loose a large amount of nitrogen at once (Stockhoff, 1994). Under a risk of herbivory, marginal costs increase with increasing nitrogen investment (Mooney and Gulmon, 1979).
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TABLE 1. Predicted daily canopy photosynthesis for a Solidago altissima stand with uniform, actual and optimal nitrogen distributions among leaves. Ka, the coefficient of nitrogen allocation; Pday, daily canopy photosynthesis; nL, nitrogen per leaf area. Ft = 4·24 m2 m–2, Nt = 5·62 gN m–2, PPFD = 43·2 mol m–2 d–1. From Hirose and Werger (1987b)
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Large returns from non-uniform distribution contrast with
Lepechinia calycina where the effect of non-uniform distribution was small
(see above; Field, 1983
). The apparent disagreement between
the result of Field and ours was solved by a model simulation.
Hirose and Werger (1987
b)
calculated the daily carbon gain for
different availabilities of nitrogen and leaf area index (
Fig. 4).
Leaf area as well as nitrogen availability were doubled
or halved relative to those found in the
Solidago altissima stand. Nitrogen was distributed either uniformly or optimally
in the canopy. The effect of non-uniform distribution was larger
in a dense than in an open stand. An open canopy showed a very
small effect of 2–3 %, similar to the result of Field
(1983)
. In reality, the Californian chaparral had an open canopy
where the darkest microsite still received 20 % of full irradiance,
which corresponds to LAI = 2·3 in our model. Plants in
a dense stand benefit more from non-uniform distribution of
nitrogen than those in an open stand, and dense canopies are
expected to develop a steeper gradient of nitrogen than open
canopies. In accordance with this expectation, a dense stand
of
Lysimachia vulgaris developed a steeper gradient of nitrogen
than an open stand (Hirose
et al., 1988
). At flowering and early
seed ripening of
S. altissima, part of the leaf nitrogen was
translocated to reproductive structures. As a result less nitrogen
was available for photosynthesis and lower leaves were dropped,
with the remaining leaves being kept within the same range as
before flowering and the gradient of leaf nitrogen becoming
less steep (Werger and Hirose, 1988
, 1991
; Schieving
et al.,
1992
b). Leaf area index of the canopy appears to be the key
regarding how nitrogen gradients will be set up. Strong gradients
of nitrogen were found to develop in dense oak forest canopies
(LAI up to 6; Wilson
et al., 2000
), while most leaves had the
same nitrogen in open oak savanna (LAI about 0·6; Xu
and Baldocchi, 2003
).
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FIG. 4. Daily canopy photosynthesis (Pday) versus total leaf nitrogen (Nt) under the optimal and uniform nitrogen allocation program. The optimal allocation was determined by eqn (10). Note different scales on the x-axis. (A) Ft = 8·48 m2 m–2; (B) 4·24 m2 m–2; (C) 2·12 m2 m–2. From Hirose and Werger (1987b).
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An important question raised from the optimal allocation theory
is what controls nitrogen distribution within the canopy. As
new leaves are produced at top of the plant, which is exposed
to full irradiance, and as young leaves are usually high in
protein content, leaf age was suggested to control the allocation
program (Field, 1983
; Field and Mooney, 1983
), although the
effect of ageing was different in extent between species native
to closed habitats and those native to open canopy habitats
(Mooney
et al., 1981
). Hirose
et al. (1989)
studied nitrogen
distribution in a stand of a monocotyledonous species,
Carex acutiformis. As this species is a rosette plant having a meristem
at the base of the plant, the youngest portion of a leaf blade
is always subject to the lowest irradiance within the canopy.
New leaf blades are produced in the centre and push older blades
outwards, thus facilitating a comparison of nitrogen in leaf
blades with different ages but exposed to the same light intensity.
It was found that nitrogen distribution was correlated strongly
with the light gradient in the canopy (
r = 0·82–0·91),
with only a small effect of leaf age (
r = 0·16–0·39).
Pons
et al. (1993)
demonstrated that this species developed
little gradient of nitrogen when leaves were illuminated uniformly
from the top to bottom. Vines provide a useful material to study
the control of leaf nitrogen, presenting leaves that can be
exposed naturally or experimentally to different irradiance
independently of leaf age. Ackerly (1992)
found that leaf nitrogen
in a tropical vine
Synogonium podophyllum was more strongly
determined by light than by leaf age. Hikosaka
et al. (1994)
subjected a vine
Ipomoea tricolor to reverse canopy-type shading
(progressively shading younger leaves) and found the more illuminated
older leaves had a higher leaf nitrogen per area than the more
shaded younger leaves. The importance of irradiance rather than
age in determining leaf nitrogen was also shown in individuals
with different heights in a dense stand (Anten and Werger, 1996
;
Anten
et al., 1998
; for review, Anten
et al., 2000
; but see
Kitajima
et al., 2002
, 2005
).
Theoretically, canopy photosynthesis is maximized when each leaf in the canopy receives irradiance in proportion to the associated photosynthetic capacity (Farquhar, 1989; see also Terashima et al., 2005):
 | (13) |
where
1, 2, 3, ... indicate different leaves. Assuming that the photosynthetic
capacity is proportional to the amount of nitrogen directly
involved in photosynthesis, Anten
et al. (1995
a)
derived the
optimal nitrogen distribution:
 | (14) |
where
Nt is the total amount of leaf canopy nitrogen,
Ft is
the total LAI, and
nb is the leaf nitrogen per area that is
not involved in photosynthesis.
Equation (14) indicates that
the photosynthetic nitrogen (
nL –
nb) decreases exponentially
as a function of
F where the proportionality constant is
K,
the light extinction coefficient [see
eqn (1)]. Nitrogen distribution
is primarily determined by the structure of the canopy (
K),
by the availability of nitrogen (
Nt), and by the amount of nitrogen
invested to structural components of the leaf (
nb). It is independent
of leaf physiology and the absolute amount of photons that plants
receive. Reduction in
nL with increasing depth in the canopy
has been observed both in agricultural crops and wild plants,
and in both herbaceous and woody species (Grindlay, 1997
).
These experimental and theoretical studies supported the hypothesis that the gradient of leaf nitrogen that develops in a canopy is a direct response to the gradient of light. Leaf age plays a secondary role in the development of the gradient of leaf nitrogen. The gradient benefits plants through the efficient use of light and nitrogen, two resources whose supply is limiting in the natural environment. Chen et al. (1993) proposed the co-ordination theory to explain nitrogen distribution in a canopy. It assumed that photosynthesis is limited by either the RuBPCase-limited rate of carboxylation (Wc) or the electron transport-limited rate of carboxylation (Wj) and that at a given light level there is a unique nL at which photosynthesis is co-limited by Wj and Wc. This co-ordination theory may explain nL decreasing with increasing depth in the canopy, but does not explain nL that changes depending on nitrogen availability as well. Optimization theory, on the other hand, predicts that nL should be distributed in proportion to light levels, and thus the distribution depends both on light and nitrogen availability in the canopy [eqn (14)].
Hikosaka and Terashima (1995) applied the optimization theory for studying light acclimation of leaf photosynthesis. They determined the pattern of N partitioning among photosynthetic components in chloroplasts that maximizes the daily carbon gain for various light environments and leaf N contents. At high irradiance, nitrogen should be allocated more to Calvin cycle enzymes and electron carriers, whilst at low irradiance, it is allocated relatively more to chlorophyll–protein complexes. Thus modelling of canopy photosynthesis with leaf nitrogen distribution enables us to scale up from chloroplast biochemistry to canopy carbon gain (Farquhar, 1989; Kull and Jarvis, 1995; Terashima and Hikosaka, 1995; De Pury and Farquhar, 1997). On the canopy photosynthesis model, Hikosaka (2003) developed a new model of leaf and nitrogen dynamics in a canopy (see Hikosaka, 2005). Canopy photosynthesis models were further applied for studying the strategy of resource use in species and individuals growing at different light and nitrogen availabilities (see below). Links between photosynthesis, nitrogen and light climate have also been implied in global-scale vegetation patterns (Reich et al., 1997; Niinemets, 2001) and used for global carbon exchange between vegetation and the atmosphere (Friend, 2001).
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CANOPY STRUCTURE OF PLANT COMMUNITIES WITH MANY SPECIES
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Most plant communities in the natural environment are composed
of a range of species differing considerably in plant height.
Tall dominant species occupy upper layers and receive a high
irradiance, while short subordinate species receive a low irradiance.
Here we may have two hypotheses: species in upper layers are
limited by the availability of nitrogen rather than by the irradiance,
and species in the lower layers are limited by the irradiance
rather than the nitrogen availability. We may then expect a
high nitrogen use efficiency and consequently a relatively low
nL in the species in the upper layers. On the other hand, the
cost–benefit hypothesis for nitrogen use predicts a high
nL in the dominant species and a low
nL in the subordinate species
in the canopy.
Hirose and Werger (1994, 1995) studied a herbaceous plant community (Thelypterido–Phragmitetum) that contained 11 species in a small area. Phragmites australis developed leaves in the uppermost layer, Calamagrostis canescens and Carex acutiformis in the next layer, and the other eight species were living in lower layers. The upper three species, comprising 95 % of the total leaf area, dominated the stand. The other eight species together had only 5 % of the total leaf area. How can those smaller species survive if they receive only small amounts of light? Hirose and Werger calculated the photon flux (number of photons per unit time) absorbed by each species (
) from its leaf area distribution in the gradient of light in the canopy, determined by the stratified clipping technique (Monsi and Saeki, 1953). They defined N as the ratio of photon flux absorption to leaf nitrogen (N):
 | (15) |
Leaves need both photons and nitrogen for photosynthetic carbon gain, and the cost–benefit theory predicted that nitrogen would be partitioned among species in proportion to the amount of absorbed photons (Anten et al., 1995a). If the photosynthetic rate is proportional to the amount of absorbed photons, N indicates in situ photosynthetic nitrogen use efficiency (photosynthesis per unit leaf nitrogen; Field and Mooney, 1986). Dividing both the numerator and denominator of eqn (15) by leaf area in each species, we have
 | (16) |
where
area is the photon absorption per unit leaf area. When
N and
nL are
plotted logarithmically on the
y- and
x-axis, respectively,
N is given as parallel contours with a slope of 1 (
Fig. 5).
Across species there was a positive correlation between
area and
nL (
r = 0·54,
P < 0·1). Nitrogen was partitioned
between species such that those capturing a large amount of
photons had high nitrogen per leaf area. This is consistent
with the prediction of the cost–benefit hypothesis. Dominants
captured a higher irradiance with leaves of higher nitrogen
content per area, as compared to subordinate species. Subordinates
received a lower fraction of irradiance, but their nitrogen
use efficiency was not smaller than those of dominants. Note
that subordinates with photosynthetic stems instead of leaves
(
Juncus and
Equisetum) are outliers.
nL is the ratio of leaf
nitrogen per mass (
nLM) to the specific leaf area (
, leaf area
per unit leaf mass):
 | (17) |
Within a species,
nL changed responding to irradiance and the
difference in
nL was caused by
nLM rather than by
, whereas
difference in
nL between species was caused mainly by different
(Hirose and Werger, 1994
). Different photosynthetic capacities
between species growing different layers have been documented
in a deciduous forest (Kull and Niinemets, 1998
).
Plants develop above-ground structures to competitively capture photons as an energy source. Tall dominant species capture a greater fraction of incident radiation, while shorter subordinate species receive a smaller fraction but nevertheless co-exist with taller species. In what characters do tall species differ from subordinate species as regards the exploitation of light resources, and are there any possible selective advantages in the characters of subordinates species? Hirose and Werger (1995) defined the absorption of photons per unit above-ground mass:
 | (18) |
where
M is plant above-ground
mass. If the above-ground mass is considered as a cost to capture
photons, then this ratio indicates an efficiency of biomass
use for capturing photons. There was some variation in
mass among species but, surprisingly, no significant difference was
found in
mass between dominant and subordinate species as groups.
Subordinate species absorbed much smaller amounts of photons,
but their efficiencies were similar to or even higher than dominant
species. Then the next question is how the subordinate species
attained their high
mass.
Dividing both the numerator and denominator of eqn (18) by leaf area, mass was separated into two components:
 | (19) |
AM is the leaf area ratio (ratio of leaf area
to above-ground mass). When
AM and
area are plotted logarithmically
on the
y- and
x-axis, respectively,
mass is given by contours
(
Fig. 6A). Across species there was a negative correlation between
the two axes (
r = 0·78,
P < 0·01). Dominants
captured high light by placing leaves at higher positions in
the canopy using the investment of a large amount of biomass
into supporting tissues and thus reducing
AM, while subordinates
receive low light but with a high
AM resulting from a limited
investment in support tissues. A decrease in the fraction of
biomass in leaves with increasing plant height has been documented
among understorey herbs (Givnish, 1982
).
AM was further separated
into leaf mass ratio (
fLM, fraction of above-ground mass in
leaf mass) and
:
 | (20) |
Subordinate species attained a high
AM by having a high
rather
than a high
fLM (
Fig. 6B). In a mixed-species stand, dominant
and subordinate species are different in the amount of resources
they acquire, but may not be different in the efficiency of
resource use, allowing them to co-exist in the stand (Hirose
and Werger, 1995
; Anten and Hirose, 1999
). Different strategies
of biomass allocation have been suggested in forest ecosystems,
where upper-storey species allocate more biomass to height growth
and understorey species more to lateral growth (Kohyama, 1987
;
King, 1990
). Sakai (1991)
showed that herbs develop different
architectures (clonal growth forms) as a result of competition
in habitats with different openness and crowding conditions.
Anten and Hirose (2003) studied canopy photosynthesis in a grassland inhabited by both C3 and C4 species. C4 species dominated at the site with their higher photosynthetic capacity. Sensitivity analysis showed that the C4 metabolism benefited the dominant species but would not benefit understorey species. Studies of canopy photosynthesis in stands with many species are limited in number. Wohlfahrt et al. (1998, 2001) modelled leaf CO2 exchange for species in mountain grassland ecosystems and incorporated the results into their vegetation–atmosphere CO2 and energy-exchange model. The model prediction of canopy net photosynthesis was verified with independent above-canopy measurements of CO2 and energy exchange.
|
SIZE STRUCTURE OF POPULATIONS IN THE PLANT COMMUNITY
|
|---|
There is a large variation in size among individuals in a stand.
According to Koyama and Kira (1956)
, size inequality increases
when the growth rate is disproportionately larger in larger
individuals, but it does not change when the growth rate of
individuals is proportional to their size. Competition among
individuals in a stand is usually asymmetric or one-sided, where
larger individuals obtain a disproportionate share of the resources
and suppress the growth of smaller individuals (Weiner, 1990
;
Hara, 1992
; Nagashima, 1999
). However, there have been few studies
that directly demonstrate that competition among individuals
is asymmetric (but see Weiner, 1986
). Anten and Hirose (1998)
applied the concept of
mass to individuals in a monospecific
stand of
Xanthium canadense, and showed that tall dominant individuals
captured light resources more than proportionately to their
size. Tall plants having higher
mass were competitively more
successful than smaller plants (see
fig. 7 in Anten, 2005
–this
issue). Small individuals responded to low light by increasing
AM, but owing to developmental constraints the plastic increase
in
AM was not large enough to compensate for the low
area. This
is quite different from the pattern observed among species in
multi-specific stands where
mass was not different between dominant
and subordinate species (
Fig. 6A; Hirose and Werger, 1995
).
Therefore, it may be concluded that individuals (having different
mass) in a monospecific stand compete for light, while different
species (having similar
mass) in a multi-specific stand tend
to co-exist with each other (see also Anten and Hirose, 1999
,
2001
, 2003
).
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|
FIG. 7. (A–C) Relative photosynthetic rate (R, daily net photosynthesis per unit above-ground mass), (D–F) daily photon absorption per unit above-ground mass (mass), and (G–I) light use efficiency ( , net photosynthesis per unit photon absorption) as a function of above-ground mass of individuals in a Xantium canadense stand. Note that R = mass x . (A, D, G) 22 July; (B, E, H) 1 August; (C, F, I) 11 August. From Hikosaka et al. (1999).
|
|
Hikosaka
et al. (1999)
determined the growth of individuals
in a dense stand of
X. canadense by applying the canopy photosynthesis
model to individual plants. Relative photosynthetic rate (
R,
photosynthetic rate per unit above-ground mass, a surrogate
for the relative growth rate) was a saturating function of plant
mass, indicating overall asymmetric competition between individuals
and symmetric competition between large individuals (
Fig. 7A–C).
R is a product of
mass and the light use efficiency (
, net carbon
gain per unit photon absorption):
 | (21) |
This equation implies that plant growth is determined by the
efficiency of light use in photosynthesis as well as by the
amount of light acquisition.
mass was higher in larger individuals
(
Fig. 7D–F), while
was highest in individuals with intermediate
above-ground mass (
Fig. 7G–I).
Berendse and Aerts (1987) defined nitrogen use efficiency (net carbon gain per unit nitrogen loss) as a product of the nitrogen productivity (Ingestad, 1979) and the mean residence time of nitrogen. Applying this concept to individuals in the stand of X. canadense, Hikosaka and Hirose (2001) showed that the nitrogen use efficiency was higher in dominants than in subordinates and that it was caused by a higher nitrogen productivity and a longer residence time of nitrogen in the former. They also showed that competition for nitrogen was less asymmetric between individuals than that for light. In a beech forest, Yasumura et al. (2002) found that canopy and understorey species were not different in leaf-level nitrogen use efficiency, where the high nitrogen productivity in the canopy species was offset by the low mean residence time of nitrogen.
|
CONCLUDING REMARKS
|
|---|
In this paper I have shown how Monsi and Saeki (1953)
developed
their theory from the work of Boysen Jensen (1932)
, and how
the model of Monsi and Saeki was furthered with the cost–benefit
hypothesis in resource use advocated by Mooney and co-workers
(1979–1983). A new method was introduced to study multi-specific
stands with respect to resource partitioning among species (Hirose
and Werger, 1994
, 1995
). This method was subsequently applied
to the analysis of resource acquisition and its use by individuals
in the stand. One of the directions that Monsi and Saeki (1953)
suggested but which has not been fully addressed is an analysis
of species' replacement in plant communities. Monsi and Saeki
(1953
; their fig. 8) beautifully described a drama of seasonal
replacement of species in the Tajimagahara plain:
Sanguisorba tenuifolia started growth early in spring and dominated the
stand but was soon over-shaded by
Phragmites australis, which
grew later but taller with a large rhizome system below ground.
Phragmites nearly monopolized the stand in the summer through
to the autumn, but this monopolization ended with a cover of
vines. We may apply the concept of resource acquisition and
use to quantitatively describe the mechanism of species replacement.
Monsi and Oshima (1955)
theoretically analysed the process of
plant succession after gap formation in a forest. Recently Werger
et al. (2002)
studied the process of regeneration and species'
replacement after excluding sika deer from a grazing sward.
They analysed the process of taller species replacing shorter
grazing-tolerant ones with respect to the species' strategy
of biomass allocation for light capture.
With the rise in the atmospheric CO2 concentration, the role of terrestrial ecosystems in the global carbon cycle becomes a critical issue (Canadell et al., 2000). Canopy photosynthesis models have been extended to evaluate the potential of terrestrial carbon fixation (Cramer et al., 1999). Ecosystem carbon exchanges are being assessed extensively with the new technique of eddy covariance (FLUXNET; Aubinet et al., 2000; Baldocchi, 2003). Tests of canopy photosynthesis models with eddy covariance data have shown that the models are producing accurate estimates of canopy photosynthesis on multiple time-scales for complex forest and crop canopies (Ruimy et al., 1995; Kramer et al., 2002). Canopy photosynthesis models are useful to predict the effect of elevated CO2 on canopy structure and function (e.g. Koch and Mooney, 1996). High CO2 may benefit leaves by enabling them to photosynthesize at a low irradiance, because the light compensation point decreases due to an increase in the initial slope (Ehleringer and Björkman, 1977; Long and Drake, 1991). The Monsi–Saeki theory on the optimal LAI suggests that the LAI would increase in a high-CO2 world. Hence, Oikawa (1987) suggested a possibility that species' diversity reduces in understorey vegetation with lowered light availabilities. Nagashima et al. (2003) demonstrated that elevated CO2 benefited dominant individuals more than subordinates and consequently increased size inequality, and Hikosaka et al. (2003) analysed the mechanisms involved in the development of hierarchy. However, Hirose et al. (1996) have shown that LAI would not increase unless nitrogen availability increased simultaneously, because the increase in the initial slope makes leaves in lower layers more nitrogen-limited (Hirose et al., 1997; see also Anten et al., 1995b). The process-based mechanistic models of canopy photosynthesis initiated by Monsi and Saeki (1953) will become more useful than ever to analyse vegetation processes and to predict future ecosystems.
|
ACKNOWLEDGEMENTS
|
|---|
I thank Niels Anten, Dennis Baldocchi, Kouki Hikosaka, Ko Noguchi,
Ichiro Terashima and Marinus Werger for comments.
|
LITERATURE CITED
|
|---|
Ackerly DD. 1992. Light, leaf age and nitrogen concentration in a tropical vine. Oecologia 89: 596–600.
Anten NPR. 2005. Optimal photosynthetic characteristics of individual plants in vegetation stands and implications for species coexistence. Annals of Botany 95: 495–506.[Abstract/Free Full Text]
Anten NPR, Hikosaka K, Hirose T. 2000. Nitrogen utilisation and the photosynthetic system. In: Marshall B, Robert
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ABSTRACT
INTRODUCTION
