Austral Ecology (2002) 27, 173–182

Survival and growth of seedlings of 12 Chilean rainforest

trees in two light environments: Gas exchange and biomass
distribution correlates
CHRISTOPHER H. LUSK1* AND ALEJANDRO DEL POZO2
1
Departamento de Botánica, Casilla 160-C, Universidad de Concepción, Concepción, Chile
(Email: clusk@udec.cl) and 2Departamento de Producción Vegetal, Universidad de Concepción,
Chillán, Chile

Abstract Mortality, growth, gas exchange and biomass distribution were measured in the seedlings of 12 Chilean
temperate rainforest angiosperm trees in two contrasting artificial light environments (150 and 12 µmoles m–2 s–1),
in order to explore life history diversity in this forest type, and examine the physiological and/or morphological
traits associated with interspecific variation in seedling performance. Gas exchange traits were measured only in
the high-light treatment (150 µmoles m–2 s–1), owing to the very small size of leaves in the low-light treatment. Relative
growth rates (RGR) in high light were strongly correlated with photosynthetic capacity (P < 0.0001). Mortality
rates in low light had a strong positive correlation with light compensation point (P = 0.007) and photosynthetic
capacity (P = 0.004). Furthermore, high-light RGR was strongly positively correlated with low-light mortality
(P = 0.001). Biomass distribution traits showed little relationship with mortality or growth within either light
level, except for a marginally significant positive correlation (P = 0.04) between leaf area ratio and mortality in low
light. In view of the large interspecific differences in final size, the weak relationships between biomass distribution
parameters and plant performance could be partially attributable to ontogenetic drift in these traits. Among taxa
with high mortality rates in low light, short-lived species (e.g. Aristotelia chilensis) had lower light compensation
points, had greater phenotypic plasticity and grew much faster in both light environments than did longer-lived
species (Nothofagus dombeyi, Weinmannia trichosperma, Eucryphia cordifolia). Results support the view that survival
of first-year seedlings in low light is not enhanced by morphological traits that maximize growth potential (e.g.
high leaf area ratio), and that leaf-level gas exchange traits have an important role as determinants of interspecific
variation in seedling performance. However, the limited range of interspecific variation observed in light compen-
sation points indicates that other traits apart from those that we measured (e.g. carbon storage) must also be involved
in seedling shade tolerance differences. The weak relationship between longevity and shade tolerance level among
our 12 species suggests that it may not be feasible to ordinate life histories of Chilean temperate rainforest trees
on a single axis of trait variation.

Key words: light compensation point, photosynthesis, relative growth rate, shade tolerance, temperate rainforest,
tree life histories.

INTRODUCTION (Kitajima 1994). Furthermore, Loehle (1988) pro-

Recent studies have produced a series of advances
in the understanding of tree life history variation in
relation to successional status. For some time, forest
ecologists have proposed that species turnover during
secondary succession results primarily from a trade-off
between growth rate in open conditions and survival
under shade (Denslow 1980; Bazzaz 1984; Huston &
Smith 1987; Canham 1989; Poulson & Platt 1989).
Such a trade-off has been empirically confirmed by
recent studies of northern temperate species (Hiura
et al. 1995; Kobe et al. 1995) and tropical species
*Corresponding author.
Accepted for publication October 2001.
duced evidence that, at least among North American
angiosperm trees, this axis of juvenile life history
variation is highly collinear with variation in a number
of key adult traits, such as age at first reproduction,
longevity and wood density.
Although research into the physiological basis of
adaptation to sun and shade has produced diverse
and sometimes apparently conflicting results, at least
part of this variation reflects real differences between
winter deciduous and broad-leaved evergreen species
(Walters & Reich 1999) and ontogenetic drift in plant
traits (Walters et al. 1993b; Poorter 1998). Traditional
explanations have emphasized the implications for
carbon balance of interspecific variation in photo-
synthetic light response curves (Grime 1965; Loach
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174 C. H. LUSK AND A. DEL POZO

1967; Boardman 1977; Givnish 1988). This view has
been challenged by work that questions the nature of
the connection between photosynthetic capacity and
dark respiration rates (Sims & Pearcy 1991), and by
comparative studies that suggest that interspecific vari-
ation in patterns of carbon allocation may be equally
or more important than gas exchange traits (Kitajima
1994; Kobe 1997). A number of comparative studies
have shown that seedlings of light-demanding species
maximize growth potential by developing a high
specific leaf area (SLA) and a high leaf area ratio
(LAR; e.g. Walters et al. 1993a; Kitajima 1994), and
rapidly commit resources to new growth, with low
allocation to storage and defence (Augspurger 1984;
Kobe 1997). However, shade tolerance (i.e. high
survival under shade) in seedlings has been linked to
conservative carbon allocation patterns, in which
growth potential is sacrificed in favour of traits that
favour persistence (Walters & Reich 1999). The risk of
damage by pathogens, herbivory and physical stresses
is reduced by the production of dense, durable, well-
defended tissues (Augspurger 1984; Coley et al. 1985;
Kitajima 1994), and recovery from such damage is
facilitated by heavy allocation to storage (Kobe 1997).
Recent reviews (Veneklaas & Poorter 1998; Walters and
Reich 1999) concluded that a survivorship advantage
in low light is not accompanied by an advantage in
growth rate: seedlings of light-demanding species often
grow faster than those of shade-tolerant associates
even in low light, reflecting the ability of the former
to lower whole-plant light compensation points by
greatly increasing LAR under shade.
Because of climatic constraints on plant structure
and function, the precise mechanisms of adaptation to
light environments differ between biomes (Walters &
Reich 1999; Coomes & Grubb 2000). Variations in
disturbance regimes are also likely to influence the
range of trait combinations that are viable in a given
biome. To date there have been very few comparative
growth and survival studies of the tree species of the
temperate forests of the Southern Hemisphere, where
life history variation may be less straightforward than
that proposed by the popular paradigm of ‘pioneer’
versus ‘non-pioneer’ species (Bazzaz 1984; Huston &
Smith 1987; Loehle 1988; Swaine & Whitmore 1988).
Although many of the light-demanding species of
southern temperate forests conform to the expectations
of short lifespan and small final size, an appreciable
number of other ‘pioneer’ species are among the largest
and longest-lived trees of this biome (Enright & Ogden
1995; Veblen et al. 1996; Lusk 1999).
The present paper reports mortality, growth, biomass
distribution and gas exchange traits for seedlings of
12 Chilean rainforest tree species, which were grown
in two different artificial light environments. We aimed
to (i) quantify the light requirements and growth rates
of juveniles of the common tree species of this forest
type; (ii) ascertain the relative importance of biomass
distribution and gas exchange as correlates of inter-
specific variation in growth and survival; and (iii) deter-
mine if short-lived early successional species and
long-lived light-demanding associates have important
trait differences at the seedling stage.
METHODS
Study species
We chose 12 species that, according to the literature,
differ widely in growth rate, successional status,
maximum size and longevity (Table 1). All of these
species are common in the Valdivian rainforest, which

Table 1. Life history data for the study species

Typical Typical Maximum Successional

maximum maximum lifespan stage where
Species Symbol Family height (m) d.b.h. (cm) (years) most common

Aextoxicon punctatum Ap Aextoxicaceae 100 30 300* Late

Amomyrtus luma Al Myrtaceae 60 20 200* Late
Aristotelia chilensis Ac Elaeocarpaceae 20 6 40 Early
Caldcluvia paniculata Cp Cunoniaceae 40 15 240 Early
Dasyphyllum diacanthoides Dd Compositae 120 35 300* Late
Drimys winteri Dw Winteraceae 80 30 250 Variable
Eucryphia cordifolia Ec Eucryphiaceae 180 40 400* Early-mid
Laurelia philippiana Lp Monimiaceae 100 30 650 Late
Myrceugenia planipes Mp Myrtaceae 30 10 260 Late
Nothofagus dombeyi Nd Fagaceae 250 45 600 Early-mid
Nothofagus nitida Nn Fagaceae 150 35 400 Early-mid
Weinmannia trichosperma Wt Cunoniaceae 150 35 730 Early-mid

d.b.h., diameter at breast height; * indicates a strong probability that maximum published ages greatly underestimate poten-
tial longevity. Data from Tortorelli 1956; Veblen 1985; Lara 1991; Veblen et al. 1995; Le-Quesne et al. 1999; Lusk 1999; I.
Martinez, unpubl. data; C. Lusk, unpubl. data).

LIGHT RESPONSES OF CHILEAN RAINFOREST SEEDLINGS
is the dominant native vegetation below approximately
800 m a.s.l. in both the Andes and the coast range of
southern Chile, between latitudes 39 and 43°S (Veblen
et al. 1983). Because of the difficulty of germinating
some of these species (Figueroa et al. 1996), small
seedlings were obtained from secondary forests and
roadbanks, standardizing size within each species
(Table 2). Ten seedlings of each species were harvested
at the outset of the experiment to determine initial dry
mass. Seed mass varies over more than three orders of
magnitude among these 12 species (Donoso & Cabello
1978), which potentially poses problems for relative
growth rate (RGR) comparisons, as RGR is signifi-
cantly influenced by plant size (Walters et al. 1993b).
Therefore, we constrained interspecific variation in
initial size to a range of less than one order of magni-
tude (Table 2).
Growth conditions
The experiment was carried out in the phytotron of
the Department of Plant Production, University of
Concepción. Seedlings were planted in 1-L plastic
pots, perforated at the base for drainage, in a mixture
of 50% washed river sand and 50% pine bark compost,
and were watered with half-strength Hoaglands
nutrient solution. In the high-light treatment, it was
necessary to transplant one of the fastest-growing
species (Aristotelia chilensis) to larger pots after approxi-
mately 4 months.
A mixture of metal halide and sodium lamps was
used to approximate the spectral qualities of sunlight.
Twenty seedlings of each species were grown on top
of two benches (the ‘high-light treatment’). These
received an average photosynthetic photon flux density
(PPFD) of approximately 130 µmoles m–2 s–1 at the
outset of the experiment, increasing as plants grew
toward the lights, to 150–300 µmoles m–2 s–1 at the
Table 2. Initial and final biomass of plants (mean  SE), grown in low light for 21 weeks, and in high light for 26 weeks
Species Initial dry mass (mg)
Aextoxicon punctatum 39.9  3.5
Amomyrtus luma 9.9  1.1
Aristotelia chilensis 25.3  4.4
Caldcluvia paniculata 11.0  1.0
Dasyphyllum diacanthoides 25.2  2.8
Drimys winteri 14.8  2.1
Eucryphia cordifolia 21.5  6.6
Laurelia philippiana 11.4  2.3
Myrceugenia planipes 31.5  4.0
Nothofagus dombeyi 13.4  1.7
Nothofagus nitida 6.1  0.6
Weinmannia trichosperma 19.0  4.2
n = 10 for initial biomass, and ranges from 3 to 17 for final biomass in low light, and from 10 to 19 for final biomass in high
light.
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175
uppermost leaves by harvest time, depending on final
height. The average PPFD experienced by the plants
in this treatment during the experiment was, therefore,
approximately 150 µmoles m–2 s–1. Another 21–22
seedlings of each species were grown beneath the
benches, the sides of which were screened with black
shade cloth. The average irradiance level beneath the
benches (the ‘low-light treatment’) was approximately
12 µmoles m–2 s–1. A 13-h photoperiod was used, mean-
ing that plants in the high-light treatment received a
daily flux of approximately 7.0 mol m–2, equivalent to
approximately 15% of that measured under open
conditions at latitude 41° during the course of a sunny
day, or approximately 60% of the corresponding
figure on an overcast day (C. Lusk, unpubl. data). In
the low-light treatment, plants received a daily flux
of approximately 0.56 mol m–2, equivalent to approxi-
mately 1.2% of total flux on a sunny day, or approxi-
mately 5% of that on an overcast day. A day–night
temperate regime of 22/18°C was used. Pots were
randomly relocated, and mortality registered, at fort-
nightly intervals.
Gas exchange measurements
During the last month of the experiment, a LI-6200
closed system infrared gas analyser was used to carry
out gas exchange measurements on five to six mature
leaves of each species in order to estimate maximum
photosynthetic capacity (Amax), dark respiration rates
(Rd) and light compensation points. In the low-light
treatment, the leaves of most species were too small to
permit gas exchange measurements, so we were able
to obtain these data for the high-light treatment only.
Because of the difficulties of controlling CO2 levels
inside the phytotron, natural sunlight was used to carry
out gas exchange measurements at 500, 100, 50, 25
and 0 µmoles m–2 s–1 for each leaf, using neutral density
Final dry mass
Low light (mg) High light (g)
69.8  11.1 2.0  0.6
24.1  3.9 2.1  0.4
101.8  35.7 55.4  3.3
45.7  13.9 27.4  1.9
58.8  6.6 5.8  1.0
20.0  4.0 2.7  1.1
18.4  1.7 12.4  0.9
21.0  4.8 3.1  0.6
68.5  5.7 1.9  0.2
15.0  0 7.1  1.0
7.8  1.5 2.2  0.3
38.0  5.5 10.9  1.4

176 C. H. LUSK AND A. DEL POZO
shadecloth to vary light intensity. Light compensation
points were estimated by interpolating between
measurements at 25 and 0 µmoles m–2 s–1. Leaf
temperatures during measurements ranged from 19
to 26°C.
Growth and biomass distribution measurements
The high-light treatment plants were harvested after
6 months. The low-light treatment plants were harves-
ted a month earlier, in order to avoid the complete
extinction of some species. Final leaf area of each plant
was measured with a LI-COR LI-3000 leaf area meter.
Plants were separated into leaves, stems and roots,
and dried at 70°C in a forced air oven for 72 h before
determining dry mass. Roots were washed thoroughly
before drying. Relative growth rates (RGR; Hunt 1982)
were estimated as:
RGR = ln (final dry mass) – ln (initial dry mass)
t (days)
Specific leaf area (SLA) was determined for the leaves
that were used for gas exchange measurements by
dividing leaf area by dry mass. Leaf mass ratio (LMR,
i.e. foliage dry mass divided by whole plant dry mass)
was also measured for each plant, as was leaf area ratio
(LAR, i.e. foliage area divided by whole plant dry
mass), which is the product of LMR  SLA.
Statistical analyses
Mortality rates were well-described by linear regres-
sions of percentage survival versus time, using JMP
Statistical Software (SAS Inc.). The relationships of
gas exchange and allocational traits to interspecific
Fig. 1. Relative growth rate (mean (SE)) of seedlings of
12 Chilean temperate rainforest trees, grown at a photo-
synthetic photon flux density of 12 and 150 µmoles m–2 s–1.
(), Low light; (), high light. Species codes as given in
Table 1.
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variation in growth and mortality were also examined
with the same software. Seedling mortality rates
were skewed even after log transformation, so non-
parametric correlations were used.
RESULTS
Growth rates
Mean RGR in high light ranged from 22 to
43 mg/g day–1 (Fig. 1). The highest growth rates were
found for Caldcluvia paniculata and Aristotelia chilensis,
two relatively short-lived species (Table 1) that are
typical of the early stages of secondary succession,
but also colonize gaps in old stands. These taxa grew
much faster than long-lived species which usually estab-
lish early in succession (e.g. Nothofagus dombeyi, Wein-
mannia trichosperma). The lowest RGR values in high
light were found for late-successional Myrceugenia pla-
nipes and Aextoxicon punctatum.
Mean RGR in low light ranged from –1 to
9 mg g–1 day–1 (Fig. 1). As was found for the high-light
treatment, C. paniculata and A. chilensis had consider-
ably higher RGR values than long-lived early succes-
sional species, one of which (Eucryphia cordifolia)
actually had negative growth in low light (Fig. 1).
However, there was no significant correlation between
RGR in high and low light (rs = 0.33, P = 0.29).
Mortality rates
Mortality rates in high light ranged from 0 to 1.7%
per week (Fig. 2), and showed no apparent trend in
relation to reputed successional status.
Fig. 2. Mortality rates (% per week) of seedlings of 12
Chilean temperate rainforest trees, grown at a photosynthetic
photon flux density of 12 and 150 µmoles m–2 s–1. (), Low
light; (), high light. Species codes as given in Table 1.
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LIGHT RESPONSES OF CHILEAN RAINFOREST SEEDLINGS 177

Mortality rates of all species were higher in low Gas exchange

light, ranging from approximately 1 to 4.5% per week
(Fig. 2). Interspecific variation was strongly skewed,
with 50% of all species dying at rates of  4% per week,
and only two late-successional species (M. planipes and
Amomyrtus luma) with mortality rates of < 3% per week.
There was no significant correlation between mortality
rates in high and low light (rs = 0.22, P = 0.48).
Biomass distribution
The biomass distribution of most species responded in
a similar way to light availability (Table 3). Specific leaf
area and LAR were much higher in the low-light treat-
ment for all species, although the degree of plasticity
varied considerably among species. The short-lived
early successional species C. paniculata and A. chilensis
had the greatest plasticity in these parameters. LMR
was also higher in low light for most but not all species.
The photosynthetic capacity (Amax) of plants grown at
150 µmoles m–2 s–1 ranged from 2.8 to 9.0 µmoles m–2 s–1
(Table 4). The highest rates were measured for the
early successional species C. paniculata, and the lowest
rates for slow-growing late-successional species,
with long-lived early successional taxa generally
having intermediate values. Interspecific variation in
light compensation points and dark respiration rates ran
approximately parallel to this trend in Amax (Table 4),
as shown by a highly significant coefficient of con-
cordance between Amax, light compensation point,
Rdarea, and Rdmass (Kendall’s W = 0.798; P = 0.0002).
Correlates of growth and mortality
Interspecific variation in RGR in low light was not
significantly correlated with any of the measured gas

Table 3. Final biomass distribution parameters (mean  SE; cm2 g–1) in low and high light (12 and 150 µmoles m–2 s–1,
respectively)

Low light High light

Species LMR SLA LAR LMR SLA LAR

Aextoxicon punctatum 0.44  0.01 278  21 122  11 0.39  0.06 139  10 54  6

Amomyrtus luma 0.50  0.05 443  58 209  28 0.63  0.02 136  3 85  3
Aristotelia chilensis 0.57  0.04 757  125 417  56 0.24  0.01 138  4 34  2
Caldcluvia paniculata 0.66  0.05 577  33 376  22 0.42  0.01 134  8 57  4
Dasyphyllum diacanthoides 0.56  0.05 335  31 189  27 0.42  0.02 188  14 78  9
Drimys winteri 0.56  0.02 385  33 213  11 0.61  0.03 142  4 87  5
Eucryphia cordifolia 0.65  0.03 498  47 316  18 0.55  0.02 130  8 72  5
Laurelia philippiana 0.59  0.05 519  37 318  48 0.47  0.02 171  8 81  4
Myrceugenia planipes 0.52  0.02 220  11 116  7 0.56  0.09 143  21 81  14
Nothofagus dombeyi 0.52  0.02 470  45 242  15 0.53  0.02 163  8 86  6
Nothofagus nitida 0.66  0.06 431  60 272  21 0.53  0.03 139  7 74  6
Weinmannia trichosperma 0.58  0.05 379  32 217  2 0.55  0.01 179  10 99  7

LMR, leaf area ratio; SLA, specific leaf area; LAR, leaf area ratio.

Table 4. Gas exchange traits (mean  SE) for plants grown at PPFD of c. 150 µmoles m–2 s–1

Amax Light compensation Rdarea Rdmass

Species (µmoles m–2 s–1) point (µmoles m–2 s–1) (µmoles m–2 s–1) (nmoles g–1 s–1)

Aextoxicon punctatum 2.8  0.3 71 0.24  0.02 3.4  0.3

Amomyrtus luma 3.7  0.5 81 0.45  0.04 6.1  0.6
Aristotelia chilensis 8.4  0.5 91 0.73  0.09 10.1  1.2
Caldcluvia paniculata 9.0  0.6 91 0.61  0.10 8.2  1.3
Dasyphyllum diacanthoides 4.8  0.3 81 0.55  0.07 10.3  1.3
Drimys winteri 4.5  0.2 91 0.64  0.10 9.1  1.4
Eucryphia cordifolia 5.0  0.5 11  1 0.68  0.04 8.8  0.5
Laurelia philippiana 4.6  0.2 71 0.56  0.04 9.6  0.7
Myrceugenia planipes 3.5  0.4 60 0.57  0.04 6.1  0.4
Nothofagus dombeyi 6.1  0.6 15  1 0.95  0.06 15.5  1.0
Nothofagus nitida 6.0  0.6 12  1 0.96  0.06 13.3  0.8
Weinmannia trichosperma 8.0  0.6 10  1 0.63  0.03 11.2  0.5

Amax, maximum photosynthetic capacity; Rd, dark respiration rates.

 14429993, 2002, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1442-9993.2002.01168.x by Universidad Austral De Chile Sistema De Bibliotecas, Wiley Online Library on [24/04/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
178 C. H. LUSK AND A. DEL POZO

exchange or biomass distribution traits (Table 5).
Relative growth rate in high light was very strongly
correlated with photosynthetic capacity (P = < 0.0001;
Fig. 3), and to a lesser extent with other gas exchange
parameters (Table 5). On the other hand, RGR in high
light was not significantly correlated with any biomass
distribution trait of plants grown in high light. However,
RGR in high light was positively correlated with
LAR (and to a lesser extent with SLA) in low light
(Table 5), implying that fast-growing species exhibited
the greatest plasticity in these traits.
Interspecific variation in mortality rates in low light
were strongly positively correlated with light compen-
sation points, photosynthetic capacity and RGR in high
light (Table 6; Figs 4,5). Dark respiration on an area
basis and RGR in low light also showed a positive
correlation of marginal statistical significance, but
there was no systematic relationship with respiration on
a mass basis (Table 6).
There was also a marginally significant correlation
of low light mortality with LAR in low light (Table 6),
but the other biomass distribution traits showed no
significant trends. Mortality rates in high light were
not significantly correlated with any gas exchange or
biomass distribution trait, nor with RGR in either treat-
ment.
Initial dry mass was not significantly correlated with
growth or mortality at either light level.
DISCUSSION
Variation in growth and mortality, and their
physiological correlates
Recent work has shown that interspecific variation
in survival (rather than growth) in low light is the

Fig. 3. Relationship between photosynthetic capacity

(Amax) and relative growth rate of seedlings of 12 Chilean
temperate rainforest trees grown at a photosynthetic photon
flux density of 150 µmoles m–2 s–1. Each point represents
a mean of six replicates for a species. Non-parametric
correlation statistics appear in Table 5.
Fig. 4. Relationship between photosynthetic light compen-
sation points of seedlings of 12 Chilean temperate rainforest
trees in high light (150 µmoles m–2 s–1), and mortality rates
in low light (12 µmoles m–2 s–1). Non-parametric correlation
statistics appear in Table 6.

Table 5. Spearman rank correlations of relative growth rate in low and high light with biomass distribution and gas exchange
traits

Low light High light

Trait rs P rs P

Phenotypes expressed in low light:

Specific leaf area 0.15 NS 0.66 0.015
Leaf mass ratio –0.15 NS 0.42 NS
Leaf area ratio 0.08 NS 0.77 0.005
Phenotypes expressed in high light:
Specific leaf area –0.10 NS –0.02 NS
Leaf mass ratio –0.34 NS –0.26 NS
Leaf area ratio –0.32 NS –0.01 NS
Amax 0.17 NS 0.96 < 0.0001*
Light compensation point 0.44 NS 0.75 0.007
Rdarea 0.39 NS 0.79 0.004
Rdmass 0.32 NS 0.62 0.050

*Significant correlations after Bonferroni correction; NS, not significant; Amax, maximum photosynthetic capacity; Rd, dark
respiration rates.
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LIGHT RESPONSES OF CHILEAN RAINFOREST SEEDLINGS 179

principal component of the phenomenon that foresters
and ecologists have long termed ‘shade tolerance’
(Augspurger 1984; Kobe et al. 1995). Our results corro-
borate field studies that have suggested that many of
the most shade-tolerant tree species of the Valdivian
rainforest belong to the family Myrtaceae, subfamily
Myrtoidae (Armesto & Fuentes 1988; Donoso 1989).
The two myrtaceous species included in the experi-
ment, Amomyrtus luma and especially Myrceugenia
planipes, had by far the lowest mortality rates in low
light (Fig. 2). However, both the Nothofagus species
included in our experiment (especially N. dombeyi) had
relatively high mortality rates in low light, in keeping
with their well-documented role as pioneer species
(Veblen et al. 1996). As was also found by Read and
Hill (1985), our results suggest that the scarcity of
Nothofagus spp. regeneration in mature and old stands
Fig. 5. Relationship between relative growth rates in high
light (150 µmoles m–2 s–1) and mortality rates in low light
(12 µmoles m–2 s–1), for seedlings of 12 Chilean temperate
rainforest trees. Non-parametric correlation statistics appear
in Table 6.
of species-rich rainforest is at least partially attributable
to their having higher light compensation points than
do most of their associates (Table 4).
Gas exchange traits appeared to be more important
than biomass distribution traits as determinants of
interspecific variation in seedling growth and survival
in the Valdivian rainforest (Tables 5,6, Figs 3–5).
Survival in low light was strongly correlated with light
compensation point and photosynthetic capacity, as
well as with RGR in high light (Table 6), whereas inter-
specific variation in RGR in high light appeared to be
driven largely by photosynthetic capacity (Table 5).
Our data are therefore consistent with the idea that an
intimate metabolic connection between photosynthetic
capacity and maintenance respiration rates is a prime
cause of the oft-cited trade-off between high-light
growth and low-light survival (Fig. 5): a high metabolic
potential is advantageous in fuelling rapid growth in
open habitats, but a liability in environments where
carbon gain is severely restricted (Grime 1965; Loach
1967; Givnish 1988; Reich et al. 1998).
In correlating low light mortality and growth with
gas exchange traits, we assume that photosynthesis and
respiration rates, if measured on low-light grown
plants, would be correlated with those resulting from
acclimation to PPFD of 150 µmoles m–2 s–1. Read and
Hill’s (1985) gas exchange data for eight rainforest taxa
(including several Nothofagus spp.) do in fact show such
a correlation for seedlings grown in two light environ-
ments that differed more widely than our two treat-
ments, although Kitajima’s (1994) data for 11 tropical
species do not. Although we were unable to obtain gas
exchange data from the low-light treatment, some
deductions can be made by examining changes in SLA
between the two light treatments. Intraspecific variation
in light compensation point and dark respiration
is partly a function of variation in SLA (Walters &

Table 6. Spearman rank correlations of mortality rates in low and high light with biomass distribution and gas exchange traits

Low light High light

rs P rs P

Phenotypes expressed in low light:

Relative growth rate –0.21 NS –0.16 NS
Specific leaf area 0.43 NS 0.01 NS
Leaf mass ratio 0.29 NS 0.11 NS
Leaf area ratio 0.60 0.0400 0.18 NS
Phenotypes expressed in high light:
Relative growth rate 0.88 0.002* –0.04 NS
Specific leaf area –0.21 NS 0.23 NS
Leaf mass ratio –0.19 NS –0.47 NS
Leaf area ratio –0.05 NS –0.19 NS
Amax 0.78 0.0040 –0.03 NS
Light compensation point 0.77 0.0050 –0.04 NS
Rdarea 0.63 0.0300 –0.01 NS
Rdmass 0.34 NS 0.12 NS

*Significant correlations after Bonferroni correction; NS, not significant; Amax, maximum photosynthetic capacity; Rd, dark
respiration rates.

180 C. H. LUSK AND A. DEL POZO
Reich 1999). The early successional species Aristotelia
chilensis and Caldcluvia paniculata, which exhibited the
greatest plasticity in this parameter (Table 3), can there-
fore also be expected to show the greatest down-
regulation of light compensation point in the low-light
treatment. In an extensive review, Walters and Reich
(1999) reported that, contrary to popular belief, the
compensation points of shade-intolerant species were
not significantly higher than those of shade-tolerant
species when grown in low light (< 4% daylight). This
reflected greater phenotypic plasticity in the light-
demanding species, which produced thinner leaves
(high SLA) in low light. Our data suggest that
these conclusions may not be applicable to all light-
demanding taxa. Although the short-lived early
successional species A. chilensis and C. paniculata had
the highly plastic allocation patterns reported by
Walters and Reich (1999), longer-lived species with
high mortality in low light (e.g. N. dombeyi and
Weinmannia trichosperma) were no more plastic in
SLA than their shade-tolerant associates (Table 3).
These longer-lived light-demanders would therefore
be expected to show less downregulation of their
light compensation points. These two groups of
light-demanding taxa therefore appear to have different
mechanisms for dealing with low-light environments.
The short-lived species are able to reduce leaf-level and
whole-plant compensation points by greatly increasing
LMR and SLA, whereas the longer-lived species,
although apparently having a less favourable instan-
taneous carbon balance, may compensate for this
disadvantage in the long term through slower leaf
turnover rates (Lusk & Contreras 1999).
Despite the statistical significance of correlations of
gas exchange parameters with mortality rates in low
light, the range of interspecific variation in light
compensation points was rather limited (Table 4),
suggesting that other traits, apart from those that we
measured, must have also influenced mortality rates.
We did not measure carbohydrate storage, but Kobe
(1997) has empirically validated an opportunity cost
model that predicts higher low-light storage allocation
in shade-tolerant species than in light-demanding
associates. In field situations, shade tolerance variation
has also been associated with differential ability to
harvest sunflecks (Chazdon 1988) and, in evergreen
forests, with differences in leaf longevity (Williams
et al. 1989; King 1994).
Specific leaf area has repeatedly been shown to be a
key trait in life history differentiation of higher plants,
and is often strongly associated with species differences
in growth rates (Poorter & Remkes 1990; Saverimuttu
& Westoby 1996; Poorter 1998). However, we found
no direct correlation between SLA and high-light
growth (Table 5) or low-light mortality rates (Table 6),
although there was evidence that fast-growing species
exhibited greater plasticity in SLA. Size-controlled
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field comparisons of Valdivian rainforest species at
the sapling stage show that short-lived pioneers have
the highest SLA values, although among longer-lived
taxa there are no consistent differences between
light-demanding and shade-tolerant species (Lusk &
Contreras 1999). This strongly suggests that the
apparent unimportance of SLA in our results was
an artefact of the large interspecific differences in final
size. Specific leaf area is known to decrease with
increasing plant size (Walters et al. 1993a; Poorter
1998), and species differed by up to a factor of six
in mean final height, and up to nearly 1.5 orders of
magnitude in mean final biomass (Table 2). A multiple-
harvest experiment (Walters et al. 1993a,b) would
therefore almost certainly detect a significant trend in
SLA among our study species.
Although LAR is also often an important correlate
of seedling growth rate differences (Poorter & Remkes
1990; Walters et al. 1993a; Veneklaas & Poorter 1998),
we found no direct relationship between LAR and RGR
in high light (Table 5). However, as for SLA, there was
evidence that LAR of fast-growing species is more
responsive to light availability, at least at the seedling
stage. Moreover, LAR did show a marginally signifi-
cant positive correlation with mortality rates in low light
(Table 6), suggesting that adaptation to shade at the
seedling stage does not parallel the typical phenotypic
response of acclimation to low light by increasing LAR.
This result concurs with the findings of reviews by
Veneklaas and Poorter (1998) and Walters and Reich
(1999) for tropical broad-leaved evergreens, but is at
variance with Callaway’s (1992) work on Californian
oaks, possibly indicating divergent mechanisms of
adaptation in rainforests and Mediterranean-type
ecosystems. As was also the case for SLA, we cannot
rule out the possibility that the low profile of LAR in
our results stems in part from the considerable final size
differences between our 12 species, as LAR is also
known to decline with plant size (Walters et al. 1993b).
However, it must also be noted that, although short-
duration experiments almost invariably find a strong
positive correlation between the LAR of small seedlings
and RGR (Veneklaas & Poorter 1998), there is evidence
that this trend is reversed during ontogeny of woody
plants, as self-shading becomes more important. Slow-
growing shade-tolerant trees usually have larger leaf
areas as adults than faster-growing light-demanders
(Coomes & Grubb 2000), and this trend is already
detectable at the sapling stage (King 1994; Lusk &
Contreras 1999).
The single-harvest structure of our experiment could
also give rise to bias in low-light growth rates. As growth
rates were measured only for ‘winners’ that survived
the full term of the experiment, bias could arise in
species that experienced high mortality in low light.
Low light growth rates may be over-estimated for
species with high mortality in this treatment, as

LIGHT RESPONSES OF CHILEAN RAINFOREST SEEDLINGS
mortality risks are higher for slow-growing individuals
in a population (Kobe et al. 1995).
Tree life history variation in southern temperate
forests
The dominant paradigm of tree life histories attributes
contrasting suites of traits to ‘pioneer’ and ‘non-
pioneer’ or ‘climax’ species (Bazzaz 1984; Huston &
Smith 1987; Loehle 1988; Swaine & Whitmore 1988).
This paradigm emphasizes strong relationships between
growth, reproduction and other life history traits in
a fashion that essentially parallels the ideas of r- and
K-selection (MacArthur & Wilson 1967). Studies of
northern temperate forests have confirmed that species
turnover during secondary succession is associated with
a trade-off between juvenile growth rates in high light
and survival under shade (Hiura et al. 1995; Kobe
et al. 1995). At least among North American angio-
sperm trees, this axis of juvenile life history variation
is closely associated with variation in a number of key
adult traits such as longevity and wood density (Loehle
1988), apparently confirming the applicability of the
prevailing paradigm for this biome.
In the Valdivian rainforest, the relationship between
lifespan and juvenile light requirements may be weaker
than that reported from northern temperate forests.
Whereas the short-lived early successional species
(A. chilensis, Caldcluvia paniculata) grew much faster
in both light environments than long-lived species that
also establish early in succession (Nothofagus dombeyi,
Weinmannia trichosperma; Fig. 1), the two groups
suffered similarly high mortality rates in low light
(Fig. 2). This evident heterogeneity among the light-
demanding taxa of the Valdivian rainforest suggests
that it may not be realistic to try to ordinate tree life
histories of Chilean temperate rainforests on a single
axis of trait variation.
ACKNOWLEDGEMENTS
We thank FONDECYT for support through grant
no. 1980084, and Javier Figueroa and two anonymous
referees for helpful comments on the manuscript.
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