Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:

Tree Physiology 16, 69--80
© 1996 Heron Publishing----Victoria, Canada

Effects of light environment and successional status on lightfleck use
by understory trees of temperate and tropical forests
MANFRED KÜPPERS,1,2 HANS TIMM,1 FRANK ORTH,1 JENS STEGEMANN,1 ROBERT
STÖBER1, HANS SCHNEIDER,1 KAILASH PALIWAL,3 K. S. T. K. KARUNAICHAMY3 and
RODOLFO ORTIZ4
1
2
3
4

Institut für Botanik, Technische Hochschule Darmstadt, Schnittspahnstrasse 10, D-64287 Darmstadt, ermany
G
Present address: Institut für Geobotanik und Botanischer Garten, Martin-Luther-Universität, Neuwerk
21, D-06108 Halle (Saale), Germany
School of Biological Sciences, Madurai Kamaraj University, Madurai 625 021, India
Escuela de Biologia, Universidad de Costa Rica, San José, Costa Rica

Received March 2, 1995

Summary Utilization efficiency (LUE) of lightflecks by
leaves increases with decreasing duration of the lightfleck, and
depends on photosynthetic induction. Sun and shade leaves
differ with respect to photosynthetic induction. Shade leaves
may become fully induced by a series of light pulses, whereas
photosynthetic induction of leaves from partial shade or full
sun depends on continuous light. Additionally, shade leaves
maintain a higher induction state over longer periods in dim
light or darkness than sun leaves. Both features are advantageous to shade leaves in a highly dynamic light environment.
We determined whether pioneer plants and late-successional
species differ in photosynthetic induction dynamics and LUE
during the establishment phase when both plant types are
growing in the shade of the understory. We also determined the
effects of shade acclimation and successional position of species on photosynthetic induction and LUE. Results from temperate and tropical rain forests indicate a trade-off between leaf
acclimation to shade and the successional position of species.
Light acclimation is important, but in deep shade, late-successional species maintain a higher induction state over longer
periods than pioneer species.
Keywords: CO2 assimilation, Costa Rica, European beech
forest, forest gap, India, photosynthetic induction, successional position, sunfleck, tropical rain forest, understory, Western Ghats.

Introduction
Most forest trees start life in the understory, either awaiting gap
formation as ‘‘oskars’’ (Silvertown 1987) or slowly but gradually growing toward the canopy. During this phase of their life
cycle, forest trees endure predominant shade more or less
frequently interrupted by light- or sunflecks. We have adopted
the definition of sunflecks proposed by Pearcy et al. (1994) as
‘‘fast excursions of high light above a dim light background.’’

We reserve the term lightfleck to the use of artificial light or a
high intensity light pulse originating from indirect light. Sunflecks and lightflecks last from seconds up to (rarely) minutes
(Chazdon and Fetcher 1984, Pfitsch and Pearcy 1989). In a
variety of forests, sunflecks contribute between 30 and 80% to
total daily photon flux, and it is likely that a large fraction of
carbon gain is attributable to sunflecks.
Highly dynamic light conditions appear to be more frequent
than conditions allowing for steady-state leaf gas exchange,
not only in the understory but also in the sun-crown, because
of effects of cloud cover, movement of leaves in wind having
impacts on leaf temperature (Roden and Pearcy 1993), and

movement of canopies. However, most of the modeling approaches (e.g., Küppers and Schulze 1985, Caldwell et al.
1986) used in scaling from leaves to region (Ehleringer and
Field 1993) are based on information obtained from steadystate conditions that clearly deviate from natural conditions
(Pearcy et al. 1994). Only a few approaches model the responses of leaf gas exchange to dynamic light conditions (Iino
et al. 1985, Kirschbaum et al. 1988, Gross et al. 1991).
The first lightflecks after darkness or a prolonged dim light
phase may not be fully utilized because photosynthetic carbon
gain by a leaf is limited by low photosynthetic induction. This
limitation is gradually removed during subsequent lightflecks
(Chazdon and Pearcy 1986a, Schneider et al. 1991) so that
lightflecks that occur later are utilized more efficiently
(Chazdon and Pearcy 1986b, Küppers and Schneider 1993).
Thus, the capacity of a leaf to assimilate carbon attributable to
a sunfleck depends strongly on the rates at which photosynthetic induction is gained and lost. Although it is known that
partial-shade and shade leaves differ in their response dynamics to sunflecks (Küppers and Schneider 1993), little is known
about photosynthetic induction dynamics in a forest understory or how efficiently co-occurring species utilize the highly
dynamic light regime.

70

KÜPPERS ET AL.

We examined leaf gas exchange in a pioneer species and a
late-successional species that were co-occurring in the understory and in an originally large but now mostly closed gap. We
also compared leaf gas exchange of two series of species of
different successional positions along gradients of light in
which (a) pioneer species were growing at higher irradiances
than successional species, and (b) pioneer species were growing in similar or deeper shade than successional species. In
addition, we compared leaf gas exchange of a series of species
of different successional positions in which all plants originated in the light regime of a refilled gap but were transplanted
to deep shade so that all species had similarly shade-acclimated leaves.

stem diameter of 2 to 3 cm. The light gradient in the canopy
was measured on an approximately 10-m tall S. petenensis tree
(25 cm diameter at 1 m above the ground) (Figure 1). Comparable measurements were also made on two 3--4-year-old trees
of the pioneer species Heliocarpus appendiculatus Turcz.
(Tiliaceae) growing in a gap, each 10 m tall (Timm 1994,
Stegemann 1994).
For an analysis of the effects of light regime versus successional position (Experiment 2), we studied a series of successional species growing in their natural sites (Table 1A, for
details see Orth 1995), where pioneer species were growing at

higher irradiances than late-successional species.
Tropical rain forest in the Western Ghats, India

Study sites and plant materials
Tropical rain forest in Costa Rica
Experiments 1 and 2 were conducted from January to March
1994 in a primary tropical rain forest at the Reserva Forestal
de San Ramon, 40 km NNW of San Ramon at 10°18′ N, 84°37′
W and 895 m above sea level. The locality is affected by NE
winds and has a mean annual precipitation of 4460 mm and a
mean annual temperature of 21 °C. It is characterized by
tropical temperatures, hyperhumidity and a relatively dry period from January to March when monthly rainfall is about
120 mm.
For Experiment 1, detailed measurements of leaf gas exchange were made on three trees of the late-successional
species Salacia petenensis Lundell (Hippocrataceae) growing
in the understory. Each tree was about 2.5 m tall with a basal

Experiment 3 was performed in a small plot of a primary
tropical rain forest at the southern end of the Western Ghats,
India, near the Kodayar Power Station (77°25′ E, 8°25′ N) at

330 m above sea level. Annual rainfall at the site is 2274 mm
and mean annual temperature is 27.4 °C. The climate is characterized by a relatively dry period from December through
March when monthly rainfall is about 30 to 80 mm. Measurements were performed in the rainy season in October 1993.
Experiment 3 was designed to determine the effect of small
light gradients on leaf gas exchange of a series of successional
species where pioneer species were growing in deeper shade
than late-successional species. Measurements were made on
early-, mid- and late-successional species (see Table 1B) growing in a small, almost refilled, 5 to 10 m wide gap that received
direct sunlight only in sunflecks. A diagramatic map of this gap
showing the positions of the individual trees and the ground-

Figure 1. Idealized scheme of the positions
of four light sensors in the canopy of an individual Salacia petenensis tree growing in
the understory and four light sensors in the
canopy of the pioneer Helicarpus appendiculatus growing at the edge of a gap in
the tropical rain forest near the research station at the Reserva Forestal de San Ramon,
Costa Rica. LS1: light sensor above crown,
LS 2: in upper crown, LS3: in lower crown,
and LS4: below crown.

LIGHTFLECK UTILIZATION IN UNDERSTORY PLANTS

71

Table 1. (A) Successional positions of selected species from the understory and refilling gaps of a tropical rain forest in Costa Rica. Species are:
Ardisia brenesii Standley (Myrsinaceae), Guarea glabra Vahl (Meliaceae), Hoffmannia dotae Standley (Rubiaceae), Jacaratia dolichaula
Woodson (Caricaceae), Justicia crenata Durkee (Acanthaceae), Myriocarpa longipes Liebmann (Urticaceae), Pentagonia costaricensis Burger &
Taylor (Rubiaceae), Plinia salticola Mc Vaugh (Myrtaceae), Psychotria graciliflora Oersted (Rubiaceae), Sloanea faginea Standley (Elaeocarpaceae), Spatacanthus hoffmannii Lindau (Acanthaceae), and Wercklea insignis Pittier & Standley (Malvaceae). Allopulus psilospermus Radlkofer
(Sapindaceae), Xylosma spp. (Flacourtiaceae) and the epiphyte Blakea gracilis Hemsley (Melastomataceae) are not included here but are included
in the light classes of Table 4A. (B) Successional positions of selected species from the gap indicated in Figure 2, growing in the understory of a
tropical rain forest of the Western Ghats in southern India. Species are: Breynia retusa Alston (Euphorbiaceae), Caryota urens L. (Arecaceae),
Chasalia ophioxyloides (Wall.) Craib (Rubiaceae), Dimocarpus longan Lour var. longan (Sapindaceae), Globba orixensis Roxb. (Zingiberaceae),
Hydnocarpus pentandra (Buch. & Ham) Oken (Flacourtiaceae), Jasminum azoricum L. (Oleaceae), Madhuca nerifolia (Moon) Lam. (Sapotaceae),
Piper argyrophyllum Miquel (Piperaceae), Pothos scandens L. (Araceae), and Vateria indica L. (Dipterocarpaceae), as well as unknown species.
Successional position
1
Very early
(A)
Myriocarpa
Wercklea

(B)
Breynia
Caryota
Malvaceae

2
Early
Myriocarpa
Wercklea
Ardisia
Hoffmannia
Jacaratia
Spatacanthus
Justicia

Breynia
Caryota
Malvaceae
Madhuca

3
Mid

4
Mid to late

5
Late

Ardisia
Hoffmannia
Jacaratia
Spatacanthus
Justicia
Psychotria
Sloanea
Guarea
Pentagonia
Plinia

Justicia
Psychotria
Sloanea
Guarea
Pentagonia
Plinia

Guarea
Pentagonia
Plinia

Madhuca
Hydnocarpus
Dimocarpus
Globba
Piper
Jasminum
Pothos
Vateria

Chasalia

Hydnocarpus
Dimocarpus
Globba
Piper
Jasminum
Pothos
Vateria
Chasalia

Malvaceae
Madhuca
Hydnocarpus
Dimocarpus
Globba
Piper
Jasminum
Pothos
Vateria

projected light classes is shown in Figure 2. Light classes were
estimated by eye (cf. Horn 1971), where light class I is comparable to an intermediate of Figures 3C and 3D, light class II
is an intermediate of Figures 3A and 3B, light class II--III is
comparable to Figure 3A, light class III is comparable to
Figure 3G, and light class III--IV is comparable to Figure 3F.

second day. Under these conditions, all plants produced several
new leaves that were completely acclimated to deep shade.
Only these newly grown leaves were taken for leaf gas exchange measurements for Experiment 4.

Temperate European beech forest in central Europe

Species were classified into five successional categories (Tables 1 and 2) on the basis of literature reports (Oberdorfer
1979, Janzen 1983, Küppers 1984, 1992, Oberbauer and Strain
1984, Oberbauer and Donnelly 1986, Pascal 1988) and our
own observations. Most of the species occur across a range of
successional states. When we plotted these categories on a
linear scale (see Figures 8A and 9), we obtained a transformation comparable to logarithmic normalization of the true time
of successional development, hence the abscissa in these figures may be treated as a quasi-logarithmic scale.

In late summer 1991, eight co-occurring species (see Table 2
and Paliwal et al. 1994) in the seedling or sapling stage were
dug out from the understory of a refilled gap in a central
European beech forest near the Botany Institute, Darmstadt
(Table 2), potted in their original soil and transferred to a
greenhouse. The plants were cultivated in a greenhouse in a
12-h photoperiod providing approximately 4% of natural daylight at day/night air temperatures of 24/14 °C and a dew point
of 20/10 °C. The plants were watered to field capacity every

Classification of successional species

72

KÜPPERS ET AL.

crimination values were determined on the same leaves used
for the gas exchange measurements. Leaf samples were oven
dried and digested with concentrated H2SO4 for 2 h at 400 °C.
Nitrogen and phosphorus in the extract were determined with
an autoanalyzer (Technicon Instruments Corp., Tarrytown,
NY). Carbon discrimination was measured by the technique
described by Osmond et al. (1975).
Results and discussion
Characterization of light fluctuations in the understory and
in a gap of a tropical rain forest

Figure 2. Idealized map of the ground-projected light gradients found
in an almost refilled gap (5 to 10 m wide) in a primary rain forest of
the Western Ghats in southern India. Individual sites of the plants
studied are indicated by crosses.

Methods
Leaf gas exchange of the plants listed in Table 2 was measured
as described by Küppers et al. (1987, 1993). All other measurements were performed in the field on uppermost fully
expanded leaves of an individual plant with a temperature- and
humidity-controlled CO2 porometer (CQP 130 and PMK-10,
modified for fast responses to CO2, WALZ, Effeltrich, Germany; CO2/H2O gas analyzer, LI-6262, Li-Cor Inc., Lincoln,
NE; for details see Timm 1994). Artificial light was provided
by Philips projection lamps (Type 13117). Photon irradiance
was varied either by varying the distance between leaf and
lamp or by using gray filters (Strand Lighting, Braunschweig,
Germany). We followed the experimental procedures described by Schneider et al. (1993), Küppers and Schneider
(1993) and Paliwal et al. (1994). All measurements were made
between 0730 and 1830 h to minimize any diurnal change in
leaf sensitivity to light gradients.
We characterized the light environment of the canopies by
means of light sensors (Hamamatsu G1118 GaAsP photodiodes, Bridgewater, NJ) (Pontailler 1990). We adopted the
light fleck utilization efficiency (LUE) definition used by
Chazdon and Pearcy (1986b).
Nitrogen and phosphate contents of leaves and carbon dis-

The late-successional species S. petenensis was growing in the
understory and the pioneer species H. appendiculatus was
growing at the edge of a 900 m2 wide gap. In the understory
above the canopy of the late-successional S. petenensis tree
(Figure 1), long-lasting sunflecks (direct sunlight) were rare,
but short sunflecks were frequent at certain times of day
(Figure 3A), and they appeared in clusters (cf. Pearcy 1988).
The number of sunflecks was significantly reduced inside the
upper canopy compared with above the canopy (Figures 3B
and 3C). No sunflecks were found below the canopy in deep
shade (Figure 3D), but there were highly dynamic light fluctuations originating from indirect, very low intensity light (not
shown but visible at a different scale of resolution). However,
total daily light below the canopy could not support a positive
daily carbon balance (cf. Timm 1994), which explains why no
leaves were present.
Light fluctuations were more pronounced and the number of
lightflecks was higher in the gap than in the understory (Figures 3E and 3F). These fluctuations were caused by cloud
cover, by movement of leaves in the wind, and by continuous
movement of whole canopies in the neighborhood of the plant
under investigation.
An analysis of sunflecks and lightflecks in terms of their
daily frequencies, maximum photon flux density (PFD) and
contribution to total daily light showed that very low PFDs
prevailed most of the time in the understory (Figure 4A). In
contrast, intermediate and high PFDs dominated in the gap;
however, low PFDs were found in the leafy part of the gap
(light sensor LS2), whereas lateral light penetrating the space
below the leafy canopy resulted in higher light intensities of 60
to 80 µmol m −2 s −1 in the lower crown (Figure 4B, light sensor
LS3) and below it (Figure 4B, light sensor LS4).
Despite these variations in PFDs, high PFDs contributed
most to the total daily light flux in both the understory and the
gap (Figures 4C and 4D), demonstrating the importance of
sunflecks in both the gap and the understory. Although very
few sunflecks reached PFDs above 1000 µmol m −2 s −1 in the
upper crown of Salacia (Figures 3B and 4A, LS2), sunflecks
contributed 45% of the daily light dose (Figure 4C, LS2). Only
in deep shade, where most plants have no leaves (LS4 in
Figures 4A and 4C and Figure 3D), did sunflecks make little
contribution to the total daily light flux.
Both the frequencies and relative contributions of different
PFDs and the duration of those PFDs that contributed most to
the total daily light flux were important for leaf gas exchange.

LIGHTFLECK UTILIZATION IN UNDERSTORY PLANTS

73

Figure 3. Diurnal courses of photon flux densities (on the clear
day of January 14, 1994) at different positions in the crowns of a
late-successional species, Salacia
petenensis (A to D) and a pioneer
species, Helicarpus appendiculatus (E to H). All PFDs were measured with the sensors arranged
horizontally as indicated in Figure 1.
Table 2. Successional positions of selected species from the understory of a temperate European beech forest near Darmstadt, Germany. Species
are: Clematis vitalba L. (Ranunculaceae), Cornus mas L. (Cornaceae), Fagus sylvatica L. (Fagaceae), Hedera helix L. (Araliaceae), Prunus avium
L. subspp. avium (Rosaceae), Robinia pseudoacacia L. (Fabaceae), introduced from North America, Rubus fruticosus agg. (Rosaceae), and Viola
reichenbachiana Jord. (Violaceae).
Successional position
1
Very early
Rubus
Robinia

2
Early
Rubus
Robinia
Cornus
Clematis
Prunus
Hedera

3
Mid

4
Mid to late

Robinia
Cornus
Clematis
Prunus
Hedera
Viola

Robinia

Prunus
Hedera
Viola
Fagus

5
Late

Hedera
Viola
Fagus

74

KÜPPERS ET AL.

Figure 4. Frequencies (% of occasions during the day) of PFDs arranged within classes (A and B),
and the relative contribution of certain PFDs to the total daily light
dose (C and D). Note the nonlinear
scales of PFD classes with special
emphasis of light in the quantum
yield region of CO2 assimilation.

From Figure 5, it is evident that for those sunflecks contributing the most to the total daily light flux, their duration decreased with increasing shade. Below the crown, lightflecks
lasting 30 to 60 s were significantly more important than
lightflecks of other durations (Figure 5C), even though short
lightflecks (1 to 5 s) are the most frequent (Pfitsch and Pearcy
1989). In the upper crown, lightflecks of intermediate duration
were important but lightflecks lasting 60 to 300 s contributed
even more to the total daily light flux. In our experiments, we
applied 30-s lightflecks at PFDs just saturating carbon uptake.
Typical leaf responses to lightfleck regimes
Lightflecks of 1 or 5 s duration at a PFD just saturating for
steady-state carbon uptake (1000 µmol m −2 s −1) resulted in a
large carbon gain (Figures 6A and 6B). Such lightflecks were
frequent in the whole crown of the pioneer species (Figures 3F
and 3G), and thus contributed significantly to total daily carbon gain. However, if the lightfleck is of short duration, most of
the carbon will be assimilated after the lightfleck, i.e., post-illuminative lightfleck CO2 fixation occurs. The longer the lightfleck, the more carbon is fixed during the light phase (Figure
6C) but at a lower light use efficiency (Pearcy 1988, Küppers
and Schneider 1993). At the end of the post-illuminative carbon fixation phase, a post-illuminative CO2 burst resulting from
photorespiration was detected (Figure 6C) (see Vines et al.
1983). A leaf that has been partially induced can be further
induced by a subsequent lightfleck, as indicated by the steady
increase in carbon gain during the light phase after the initial

induction step (Figure 6D). Even in lightflecks as short as 1 s,
a partial induction may take place (Küppers and Schneider
1993). The rate of induction differed between sun and shade
leaves. The shade leaves of the late-successional S. petenensis
became fully induced in response to pulses of light, whereas
half-shade and sun leaves of the pioneer H. appendiculatis
only became fully induced when exposed to continuous saturating light (cf. Küppers and Schneider 1993). Additionally,
shade leaves maintained a higher induction state longer at
lower PFDs than sun leaves, and therefore, shade leaves exhibited a higher LUE than sun leaves (Figure 7).
The relative contribution of post-illuminative CO2 fixation
to total carbon gain attributable to a lightfleck increased with
decreasing duration of the lightfleck, and it also increased with
decreasing induction state (cf. Figures 7C and 7D). Post-illuminative carbon gain contributed more to the shade leaves of
the late-successional Salacia than to the sun leaves of the
pioneer Heliocarpus and may be an effect of either shade
acclimation or successional status of the plants.
Depending on the time of measurements, we observed clear
differences in leaf responses to transient light conditions with
fastest rates of induction and slowest rates of induction loss at
night and minimum variability during the day (Table 3).
Effect of partial shade gradients versus successional ranges
of species
Experiment 2 was undertaken to determine whether the light
environment contributes more to leaf responses than does the

LIGHTFLECK UTILIZATION IN UNDERSTORY PLANTS

75

Figure 5. Relative contribution of lightflecks of certain durations to the
total daily light dose in the understory (A) above the crown, (B) in the
upper crown, and (C) below the crown of a Salacia petenensis sapling.

successional position of species. Based on data from the tropical rain forest in Costa Rica, where pioneer species were
growing in the open and late-successional species were growing in half to full shade (Table 4A), we found a significant
negative correlation between light class and successional position of the species. The negative correlation arises because, as
a result of light acclimation, photosynthetic capacity was
highly positively correlated with the light class in which the
leaves were grown (Table 4B). Except for the fraction of

Figure 6. Responses of CO2 assimilation to lightflecks differing in
duration at saturating PFD (1800 µmol m −2 s −1). (A to C) Heliocarpus
leaf in fully induced state, (D) Heliocarpus leaf in a partially induced
state. Leaf temperature was about 27 °C and leaf-to-air water vapor
concentration gradient was about 10--15 mmol mol −1.

76

KÜPPERS ET AL.

Figure 7. Lightfleck utilization efficiency in relation to photosynthetic induction (A and B) and the
increase in the amount of post-illuminatively fixed carbon (after a
30-s lightfleck) with increasing
dark phase prior to the lightfleck
(C and D).

Table 3. Photosynthetic induction and CO2 assimilation responses of two understory species at the Western Ghats site to transient light at different
times of the day and night.
Pothos scandens
Time (h)
Date (October 1993)
Time to reach 50% induction (min)
Time to reach 100% induction (min)
Fully induced leaves
Photosynthetic capacity
at ambient CO2 (µmol m −2 s −1)
Total CO2 gain attributable to 30-s
lightfleck (µmol m −2 lightfleck −1)
LUE (%) attributable to 1-s lightfleck
LUE (%) attributable to 10-s lightfleck
LUE(%) attributable to 30-s lightfleck
Time to lose 50% induction (min)

Hydnocarpus pentandra

0530
27

1240
26

2150
26

0830
26

1630
26

0120
27

6
24

50
70

8
26

22
49

21
38

9
27

0.4

0.9

0.7

2.9

1.9

--

73

61

93

109

--

107

120
112
103
39

124
111
108
32

122
117
115
37

134
119
108
28

138
112
72 (?)
14

195
120
112
31

post-illuminative carbon gain, none of the other response parameters of CO2 assimilation was correlated with successional
position. This lack of correlation also appears to be a result of
light acclimation rather than an effect of successional position.
The fraction of post-illuminative carbon gain declined significantly with increasing light class (cf. Figures 7C and 7D).
Thus, under natural conditions, the correlations between photosynthetic parameters (both steady-state and dynamic) and
the light class in which the plant grew were higher than the
correlations between photosynthetic parameters and the successional position of the species.
In a second data set, which originated from an almost re-

filled gap in the tropical rain forest of the Western Ghats, India,
where pioneer species were growing in similar or deeper shade
than late-successional species, we found that the light class of
an individual’s site did not correlate with the individual’s
successional position (Figure 8A). In this refilled gap, the light
environment of a plant significantly affected its rate of photosynthetic induction (Figure 8B), whereas successional position
had no influence (Table 4B). Light acclimation clearly affected
photosynthetic capacity (per unit of leaf area), the rate of
photosynthetic induction and the minimal induction state,
which was highest in the shade plants (significant negative
slope, Table 4B).

LIGHTFLECK UTILIZATION IN UNDERSTORY PLANTS

77

Table 4. (A) Correlations of parameters of dynamic photosynthesis with successional positions of species or the light classes at the individual plant
sites for species in the understory of a tropical rain forest in Costa Rica. LUE = Lightfleckutilization efficiency, LQY = lightfleck quantum yield,
and WUE = water use efficiency. (B) Correlations of parameters of dynamic photosynthesis with successional positions of species or the light
classes at the individual plant sites (see Figure 2) for species in the understory of a tropical rain forest in the Western Ghats, India.
Dependent variable

r

P

Significance

Slope and significance

(A)
Successional position of species
Light class of plant site
Photosynthetic capacity
Time to reach 50% induction
Time to reach 100% induction
Time to lose 50% induction
Induction state after 1 min darkness
Minimal induction state (after 20 min)
% Post-illuminative CO2 gain
LUE in 3 s of light
LUE in 30 s of light

0.290
0.396
0.015
0.119
0.019
0.169
0.239
0.489
0.179
0.055

0.037
0.0037
0.918
0.409
0.896
0.242
0.094
< 0.001
0.204
0.701

*1
****
ns
ns
ns
ns
(*)
****
ns
ns

−*
− ****
− ns
− ns
− ns
+ ns
+ (*)
+ ****
+ ns
− ns

Light class of individual plant site
Photosynthetic capacity
Time to reach 50% induction
Time to reach 100% induction
Time to lose 50% induction
Induction state after 1 min darkness
Minimal induction state (after 20 min)
% Post-illuminative CO2 gain
LUE in 3 s of light
LUE in 30 s of light

0.655
0.023
0.012
0.548
0.253
0.341
0.495
0.121
0.103

< 0.001
0.867
0.928
< 0.001
0.056
0.009
< 0.001
0.357
0.433

****
ns
ns
****
(*)
***
****
ns
ns

+ ****
− ns
− ns
− ****
− (*)
− ***
− ****
− ns
− ns

(B)
Successional position of species
Light class of plant site
Photosynthetic capacity
Phosphate content
Nitrogen content
δ13C
Time to reach 50% induction
Time to reach 100% induction
Time to lose 50% induction
Induction state after 1 min darkness
Induction state after 10 min darkness
Minimal induction state
% Post-illuminative CO2 gain
LUE in 3 s of light
LUE in 30 s of light
LUE (30 s) after 1 min darkness
LUE (30 s) after 20 min darkness

0.016
0.149
0.091
0.286
0.097
0.171
0.277
0.434
0.255
0.108
0.061
0.293
0.323
0.416
0.257
0.236

0.922
0.518
0.587
0.091
0.557
0.078
0.084
0.021
0.132
0.545
0.721
0.087
0.099
0.008
0.102
0.139

ns
ns
ns
(*)
ns
(*)
(*)
*
ns
ns
ns
(*)
(*)
***
ns
ns

− ns
− ns
+ ns
+ (*)
+ ns
+ ns
+ (*)
+*
+ ns
− ns
+ n. s
− (*)
− ns
− ***
− ns
− ns

Light class of individual plant site
Photosynthetic capacity
Phosphate content
Nitrogen content
δ13C
Time to reach 50% induction
Time to reach 100% induction
Time to lose 50% induction
Induction state after 1 min darkness
Induction state after 10 min darkness
Minimal induction state
% Post-illuminative CO2 gain
LUE in 3 s of light
LUE in 30 s of light
LUE (30 s) after 1 min darkness
LUE (30 s) after 20 min darkness

0.669
0.300
0.195
0.246
0.536
0.569
0.476
0.055
0.281
0.330
0.219
0.325
0.033
0.169
0.148

0.001
0.065
0.130
0.098
0.001
< 0.001
0.009
0.774
0.087
0.045
0.136
0.086
0.839
0.085
0.490

****
(*)
ns
(*)
****
****
***
ns
(*)
*
ns
(*)
ns
(*)
ns

+ ****
+ (*)
+ ns
− ns
+ ****
+ ****
− ***
− ns
+ ns
−*
− ns
− (*)
− ns
− ns
− ns

1

Abbreviations: ns = not significant, (*) = 0.10 >P > 0.05, * = 0.05 ≥ P > 0.025, ** = 0.025 ≥ P > 0.01, *** = 0.01 ≥ P > 0.005, **** = 0.005≥ P.

78

KÜPPERS ET AL.

In the almost refilled gap at Western Ghats, there were only
weak correlations between successional position of the species
and the dynamic response parameters studied (Table 4B).
Thus, we observed significant correlations between successional position and nitrogen content, time to reach 100%
induction, % post-illuminative CO2 gain, and LUE in response
to 30 s of light (Table 4B). All of these correlations, which
contrast with those normally obtained, are a consequence of
light acclimation in the reverse situation, i.e., the pioneer
species were growing in similar or deeper shade than the
late-successional species. However, in agreement with the
observation of Poorter and Oberbauer (1993) and our observations at the Costa Rica site, the late-successional species maintained a higher induction status longer than the pioneer species
(Table 4B). We also observed highly significant positive correlations between photosynthetic capacity and phosphate or nitrogen content (P < 0.0005 and P = 0.017, respectively), and a
negative correlation between photosynthetic capacity and δ13C
values (P = 0.001; data not shown).
Effect of successional range of species originating from the
same understory and cultivated in identical shade

Figure 8. (A) Correlation between the light classes of individual plants
of several species growing in the gap depicted in Figure 2 and their
successional positions. (No significant correlation (ns) was found.)
(B) Correlation between the time necessary for leaves to become half
induced (by a step from darkness to continuous saturating light) and
the light classes of individual plants of several species growing in the
gap depicted in Figure 2.

Results from Experiments 1--3 clearly indicate the importance
of the light regime relative to the successional position of the
species on leaf responses. To determine whether successional
position has any detectable influence on leaf gas exchange, we
selected plants growing in the understory of a refilled gap in a
beech forest, potted the plants in their original soil and maintained them in shade in a greenhouse. We then made measurements on the newly grown shade leaves. There was no
correlation between photosynthetic capacity, minimal induction state and successional position of species. All other parameters studied were significantly or weakly significantly
correlated (Table 5). Thus, rates of induction in high PFDs
were faster in late-successional plants than in early-successional plants (Figure 9A, significant negative slope, and Table
5), whereas rates of induction loss in low PFDs were slower in
late-successional plants than in early-successional plants (Figure 9B, significant positive slope). The minimum saturating
light required for steady-state conditions was lower and lightfleck quantum yield, LQY (comparable to LUE; see Küppers

Table 5. Correlations of parameters of dynamic photosynthesis with successional positions of species for species from the understory of a temperate
European beech forest. LQY = Lightfleck quantum yield, and WUE = water use efficiency.
Dependent variable

r

P

Significance

Slope and significance

Successional position of species
Photosynthetic capacity
Time to reach 50% induction
Time to reach 100% induction
Time to lose 50% induction
Induction state after 1 h of dim light
Minimal saturating light
Total CO2 gain (30-s lightfleck)
LQY (30-s lightfleck)
WUE (30-s lightfleck)

0.083
0.474
0.378
0.473
0.243
0.522
0.165
0.280
0.442

0.713
0.026
0.076
0.027
0.142
0.013
0.085
0.085
0.041

ns1
*
(*)
*
ns
**
(*)
(*)
*

− ns
− (*)
− (*)
+*
+ ns
− **
− ns
+ (*)
− **

1

Abbreviations: ns = not significant, (*) = 0.10 >P > 0.05, * = 0.05 ≥ P > 0.025, ** = 0.025 ≥ P > 0.01, *** = 0.01 ≥ P > 0.005, **** = 0.005≥ P.

LIGHTFLECK UTILIZATION IN UNDERSTORY PLANTS

79

ally lead to advantages in carbon gain (cf. Cowan 1982).
Poorter and Oberbauer (1993) came to a similar conclusion
based on transplantation experiments with a tropical pioneer
species and a late-successional species.
Acknowledgments
We thank the Institut Français de Pondichéry, Madras, for help in
identifying species from the understory of the Western Ghats and Prof.
Dr. Hubert Ziegler, Munich, for the carbon discrimination analyses.
We also gratefully acknowledge support from the Deutsche Forschungsgemeinschaft to M.K. and K.P. and a fellowship by the Studienstiftung des Deutschen Volkes to H.S. We very much appreciate the
help provided by Prof. R.W. Pearcy (UC Davis) while on a visit to
Darmstadt.
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Figure 9. Significant correlations between (A) the time necessary for
leaves to become half induced (by a step from darkness to continuous
saturating light) and the successional position of species, and (B) the
time available before induction drops from 100 to 50% after a step
from high light to darkness in plants from a temperate European forest.

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light regime on the leaf response patterns to lightflecks.
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acclimation is important, but in deep shade, late-successional
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