Journal of Tropical Ecology (2005) 21:317–328. Copyright © 2005 Cambridge University Press
doi:10.1017/S0266467405002269 Printed in the United Kingdom
Pair-wise competition-trials amongst seedlings of ten dipterocarp species;
the role of initial height, growth rate and leaf attributes
E. V. J. Tanner∗1 , V. K. Teo∗ , D. A. Coomes∗ and J. J. Midgley†
∗ Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK
† Botany Department, University of Cape Town, P. Bag Rondebosch, 7701 South Africa
(Accepted 7 October 2004)
Abstract: To investigate whether seedlings of ten dipterocarp species differed significantly in terms of growth and
mortality or whether species were not significantly different and could be considered ecologically similar, seedlings
were grown, two per pot, in two experiments: (1) where the two seedlings were of equal height (30 cm); and
(2) where one seedling was 10 cm shorter than the other. Seedlings were grown in a shade house with 15% abovecanopy light in a 50:50 forest soil–sand mixture and were watered frequently; pots were placed so that seedling
density was 130 seedlings m−2 of ground. In the first experiment there were 45 pairwise combinations of species when
seedlings were 30 cm tall (AB, AC, AD, . . . . BC, BD . . . IJ; where A, B, C . . . J signify different species); each combination
was replicated 10 times so there were 450 pots with 900 seedlings. In the second experiment there were 100 pairwise
combinations of species and size e.g. Aa (30 cm A with 20 cm a), Ab (30 cm A with 20 cm b), each combination was
replicated 10 times hence there were 1000 pots with 2000 seedlings. After 22 mo 79% of the initial 2900 seedlings
survived; on average they had grown 42 cm (i.e. to 72 cm tall from their initial 30 cm). The most frequent outcome of
competition-trials between different sized individuals (784 of 1000 trials) was that the initially taller seedling of each
pair ‘won’ (it was the taller or surviving seedling). When 900 of these trials (setting aside, Aa, Bb, Cc etc.) were analysed
as 45 comparisons between species with different sized individuals (Ab and aB are one interspecific comparison for
these purposes), initial height determined the outcome in 23 cases (even in some competitions between light hardwood
species and heavy hardwood species); in 6 cases a species (mostly light hardwoods) behaved as a ‘dominant’ – they
usually won even if they were smaller initially. We found few significant differences between species in: initial seedling
heights; leaf nitrogen concentrations; and specific leaf areas when they were grown in similar conditions, and these
attributes were not correlated with growth rates. The similarity of seedlings of different species meant that often a
height difference of just 10 cm was enough to determine the outcome of a pairwise competition-trial in high seedling
densities and light equivalent to that in forest gaps.
Key Words: competition, Dipterocarpaceae, Dryobalanops, Hopea, Parashorea, seedlings, Shorea, size, tropical trees
INTRODUCTION
The understanding of determinants of forest dynamics
and species co-existence can be polarised into the
following two extremes – chance versus niche (Brokaw &
Busing 2000). Chance is the most important determinant
of success in the neutral model; interspecific differences
(such as for minimum or maximum light requirements)
are considered to be small and thus most species fall within
a few broad guilds. These differences are considered to
be relatively unimportant in explaining dynamics and
1 Corresponding author. Email: [email protected]
co-existence (Hubbell 2001); instead, chance events, such
as those related to the vagaries of phenology, predation,
or dispersal and how these may limit seedling recruitment
in gaps are thought to be more important (Hubbell et al.
1999). In contrast, in the more traditional model, speciesspecific differences are considered significant and are
important in explaining dynamics and co-existence. In
this model, a diversity of gap sizes and frequencies is
needed to facilitate co-existence (see review Sheil &
Burslem 2003). To test these ideas forest ecologists are
asking questions such as (1) are there niche differences
amongst forest trees? and (2) what are the main factors,
both biotic and abiotic, which determine ecological
318
success? An example of meaningful niche differences
would be evidence that a species had winning growth
in a particular gap size. Such differences should be related
to predictable physiological (e.g. rates of photosynthesis
at light saturation, Asat ), morphological (e.g. specific leaf
area, SLA) or allocational attributes (e.g. wood density).
On the other hand, the species recruiting most successfully
at any one time may, by chance, have had superior
access to gaps; for example, they may have happened
to have large numbers of seedlings and/or some tall
individual seedlings. We realise that such differences in
height and numbers may not be due to chance alone;
there is no strict separation of niche-caused and chancecaused differences, for example particular seedlings in
the understorey may be tall because they grew for a
long time, or because they were never hit by branch
falls.
Despite forest ecology being relatively well known in
South-East Asia, especially of the dominant canopy family
the Dipterocarpaceae, it is still not clear to what extent
dipterocarps are ecologically different and persist because
of these differences. One example of a study that does show
ecological differences is that of Brown & Whitmore (1992)
and Whitmore & Brown (1996) who followed seedling
growth in forest over 77 mo in sites ranging from large
gaps to under closed canopies. After 40 mo, the tallest
seedlings in gaps were those that had been in the advance
regeneration and so were mostly individuals of shadetolerant species. But after 53 mo individuals of fastergrowing, different, species had overtopped the shade
tolerators. These faster-growing, more light-demanding,
species continued to grow, and 10 y after the creation
of the original gaps were ‘like telegraph poles’ (T. C.
Whitmore pers. comm.). Brown & Whitmore’s experiment
is evidence for the existence of functional groups; ranging
from, on the one hand, a group of slow-growing, shadetolerant species that maintain a seedling bank, to a
group of faster-growing, more light-demanding species
with small seedling banks. The faster-growing species had
lower wood density and Whitmore and others promoted
the use of wood density as a way of classifying species into
ecological groups.
However within the general framework of functional
groups it is not clear whether species in the same group
have subtle ecological differences which determine the
outcome of competition or whether other factors, such
as differences in seedling height, (which may be partly
influenced by chance events) and position of seedlings
relative to each other are important in determining the
outcome of competition.
In contrast to the conclusions of Whitmore & Brown,
other workers have failed to find a correlated suite of
characteristics that one would expect from species in a
functional group. Barker et al. (1997) found that the
rate of photosynthesis at light saturation (Asat ) of several
TANNER ET AL.
dipterocarps was not correlated with rates of height or
diameter growth. They also argued that if species with
inherently high Asat were overtopped they would be
prevented from achieving these high Asat levels. Thus,
they conclude that stochastic events, including the spatial
arrangement and height differences could be critical to
deciding the outcome of competition to fill a gap.
In order to investigate further whether there were
ecologically important differences between dipterocarp
species or whether many were functionally, ecologically
similar we used a shade-house experiment to answer
the following questions: (1) are there any competitive
hierarchies between species and, if so, are these
maintained when initial height of competing seedlings is
varied?; and (2) which leaf characteristics best predict the
order in competitive hierarchies? There have been many
studies of seedling dynamics in dipterocarp forests but no
detailed studies published of which seedling wins when it
is in direct competition with its near neighbours. All the
published research reports changes in relative abundance
in populations of seedlings in forest plots (e.g. Dellisio et al.
2002), or changes relative to densities of adults and
seedlings (Blundell & Peart 2004) but it is not clear which
if any of the seedlings were competing with each other.
The most relevant studies of interspecific competition (in
the current context) is that by Webb & Peart (1999)
who showed density dependence of seedling growth and
mortality across many species in forest dominated by
dipterocarps, but even in that study density dependence
could be due to herbivory and pathogens as well as
(or even to the exclusion of) competition for resources.
While very interesting, these results tell us little about the
competition between near neighbours. There have also
been several shade-house studies of seedling growth that
make comparisons between seedlings, but none of these
was designed to study interspecific competition, indeed
some were designed, for good reasons, to specifically
exclude it (e.g. Ashton 1995). We are not suggesting
that these earlier studies are not interesting or relevant
to understanding the maintenance of species diversity,
just that they do not address the process of competition
between seedlings that are near neighbours, something
that is potentially very important in determining the
overall composition of the seedling flora and thus, later,
the composition of the larger trees in the forest.
Our shade house experiment was designed to study
interspecific and intraspecific competition. We chose to
use a shade-house rather than forest gaps, in order to
minimise the large variation in light climate that occurs
in gaps. In addition, our shade-house study allowed us to
standardize the soil and to water the plants, eliminating
further sources of variation in plant growth, we were thus
able to concentrate on the effects of differences in species
and differences in the size of seedlings. Our experiment
pitted seedlings of different species and often different sizes
Competition among dipterocarps
319
Table 1. The study species, their wood densities (Meijer & Wood 1964 and pers. comm. foresters at Innoprise Face Project), LHW = light hard
wood; MHW = medium hard wood, HHW = heavy hard wood; mean leaf nitrogen (N) concentrations, mean specific leaf areas (SLA) and mean
leaf thicknesses, in the youngest fully mature leaves collected from tall plants in our shade-house experiment (n = 10 for each mean).∗ indicates
significantly different from other species. Nut dimensions from Ashton (1982).
Species
Dryobalanops lanceolata Burck
Shorea beccariana Burck
Shorea leprosula Miq.
Shorea fallax Meijer
Shorea johorensis Foxw.
Parashorea malaanonan Blanco
Parashorea tomentella Meijer
Shorea falciferoides ssp.
glaucescens (Meijer) Ashton
Shorea seminis (De Vriese) van Slooten
Hopea sp.
Timber
density
N
(mg g−1 )
SLA
(cm2 g−1 )
Leaf thickness
(µm)
Product of mean
nut dimensions (cm3 )
Initial seedling height
(cm) of taller seedlings
mean ± SE
MHW
LHW
LHW
LHW
LHW
LHW
LHW
14.5
14.1
15.5
19.0
14.3
14.6
16.7
119.0
131.1
156.6
126.0
130.3
118.8
116.0
175∗
78
84
73
99
90
96
8.0
31.4
3.4
2.7
3.9
3.3
8.0
30.6 ± 1.8
29.8 ± 2.8
31.7 ± 2.5
30.9 ± 2.3
31.2 ± 2.2
31.0 ± 2.2
30.9 ± 2.4
HHW
HHW
HHW
13.8
16.9
14.9
103.0
127.6
166.8
105
90
109
3.3
1.0
–
31.0 ± 2.4
30.6 ± 2.6
30.9 ± 2.6
against each other, using pairs of plants in pots, with the
pots closely spaced. For the tall seedlings, competition was
mostly below ground with the other seedling in the pot
(if they suffered competition). For the shorter seedlings,
competition with the taller seedling in the same pot, and
with taller seedlings in surrounding pots, was for light;
and potentially with the taller seedling in the same pot,
for nutrients. Watering eliminated potential competition
for water.
METHODS
The study took place in a shade-house at the Innoprise
Face Project about 10 km from Danum Valley Field
Centre (4.58◦ N, 117.48◦ E) in Sabah, Malaysian Borneo.
We used ten species, six light hardwoods, one medium
hardwood and three heavy hardwoods (Table 1). Based
on their wood density we would expect the light hardwood
species to be relatively fast growing, and the medium
and heavy hardwoods to grow more slowly and be more
shade tolerant. There are not many studies of the growth
and ecology of these species but what exists does support
the interpretation from wood density. Shorea beccariana,
a light hardwood, was the tenth fastest growing tree
species (and the fifth of 11 Dipterocarpaceae) in a study
of 198 species in lowland forest in north-east Sabah
(Nicholson 1965). Shorea fallax, Shorea johorensis and
Parashorea malaanonan (all light hardwoods) all had high
relative growth rates of trunks of small trees at Danum
in Sabah (Table 5 in Newbery et al. 1999). Furthermore,
seedlings of S. leprosula and S. johorensis had relatively
high growth and mortality rates in natural populations
in nearby forests (Still 1996). There are fewer studies of
medium and heavy hardwoods, probably because they are
less important commercially, but two studies of seedlings
give (partial) support for the idea that seedlings of light
hardwoods grow faster than medium hardwoods in small
and medium-sized gaps. In the first Whitmore & Brown
(1996) compared seedling growth of one medium (Hopea
nervosa) and two light hardwoods (Parashorea malaanonan
and Shorea johorensis); S. johorensis grew much faster
than H. nervosa, but the P. malaanonan grew only as fast
as H. nervosa; a result put down to apical herbivory in
the P. malaanonan (Whitmore & Brown 1996). In the
second study, Zipperlen & Press (1996) showed that the
light hardwood Shorea leprosula grew taller and had a
higher relative growth rate than the medium hardwood
Dryobalanops lanceolata in the higher light environments
(10–24% canopy openness). Thus the ecology of these
species, as far as it is known, is that the light hardwoods
are more light-demanding as seedlings and are faster
growing both in height as seedlings in gaps and in girth as
young trees, and the medium and heavy hardwoods are
more shade tolerant as seedlings and grow more slowly
as seedlings and young adults.
Seeds were collected locally during the masting of
September 1996, germinated in pots of forest topsoil
in a deep-shade shade house where the seedlings were
kept until they were used for our experiment in July
1997, when they were about 30 cm tall. Seedlings were
potted on into 8.5-cm-diameter and 50-cm-deep straightsided pots filled with a 50:50 mix of forest topsoil and
river sand. Two seedlings were planted in each pot and
pots were placed so that seedlings were at a density of
130 m−2 of shade-house ground area (not pot surface
area). The pots were placed in a ‘light shade’ shade house
with neutral shade allowing passage of c. 15% of daylight
(measured over 24 h with two Skye Datahog PAR sensors,
one above the shade house one in the shade house), which
is similar to the total daily PPFD in a ridgetop gap in forest
with dipterocarps in Sri Lanka (Gunatilleke et al. 1997).
Watering was frequent enough to prevent wilting and
certainly to prevent drought mortality.
320
Two experiments; XY versus Xy
Throughout the paper X means a large individual, and x
a small individual, of a species, and Y means a large, and
y a small individual of another species. X, x and Y, y are
thus general terms and can refer to any of the ten species.
Pairwise competition-trials were made where both
species had similar initial height – about 30 cm (species
X vs. species Y, symmetrical competition-trials) and
also where one individual was 10 cm shorter (so they
were 20 cm tall) than the other (X vs. y, asymmetrical
competition-trials). To create the 10-cm height difference,
individuals that were 30 cm tall were planted 10 cm
deeper into a pot i.e. with soil–sand mix 10 cm up the stem.
Since most of the leaves of all species were at the apex
of the stem, this did not involve burying any leaves.
This partial burial had no impact on growth (separate
experiment, data not presented). We had 10 replicates
of the following combinations: XY (we did not study
XX, hence 450 pots = 900 seedlings) and Xx, Xy, xY
(1000 pots = 2000 seedlings). At five times during the
experiment we measured seedling heights (in July 1997
and in August/September 1997; February 1998; August
1998 and May 1999 – 22 mo in total), noted mortality
(almost no mortality occurred within the first few mo of
the experiment) and rerandomised the location of pots.
We did not measure biomass, it is likely that height and
biomass were highly correlated; for example the results
from the study of dipterocarp seedlings grown in shade
houses by Gunatilleke et al. (1998) show that height was
correlated with biomass (r = 0.63, P = 0.002). It is probable that height growth is the major parameter determining competitive outcomes amongst forest seedlings
growing in gaps – but not those growing in the very
low light of the understorey (Blundell & Peart 2004).
We report growth and ‘wins’; of the two seedlings in a
pot, a seedling was the winner (of the two in the pot) if
it was taller, or the survivor, after 22 mo. In only 19 of
the 1450 pots were the two seedling heights within 1 cm
of each other, these were deemed to have ‘drawn’. In a
further 85 pots both seedlings had died, in those pots,
heights in the previous recordings were used to decide
which was the winner; this method of scoring leads to
the situation where the number of ‘winners’ is greater
than the number of survivors in three instances. For the
analysis a win scores 1, a draw 0.5, a lose 0.
To determine whether the initial difference in height
between two seedlings was increasing or decreasing with
time we calculated the slopes of the regressions of the
height ratios plotted against time, for the 641 pots with
two seedlings alive in May 1999, which initially had
dissimilar-sized seedlings, and compared the distribution
with a standard normal distribution to determine whether
the population of slopes was significantly different from
zero.
TANNER ET AL.
To determine important (Wright et al. 2004) morphological and physiological characteristics we collected, in
August 1998, the first or second (from the top) fully
expanded leaf from ten randomly chosen tall individuals
of each species for determination of specific leaf area (leaf
area measured using Delta T meter) and nitrogen (after
digestion in sulphuric acid and hydrogen peroxide with
mercury catalyst, see Tanner et al. 1992 for methods).
Similar leaves were preserved in formalin acetic alcohol
and, after sectioning, leaf thickness was measured.
Statistical analyses and interpretation
The outcomes of the pairwise competition-trials: 0 (a lose),
0.5 (a draw) or 1 (a win) were analysed by goodness-offit tests by comparing the actual distribution to expected
distribution calculated from binomial distributions. The
outcome of competition in each pot can be likened to
tossing a coin; if you toss it 10 times the average result
will be five heads and five tails, equivalent to five wins
for one species and five wins for the other; over a large
number of tests a binomial distribution results. We tested
whether our use of 0.5 for a draw and, in the case where
both seedlings in a pot were dead, assigning a winner
from previous recordings, affected the outcome of our
statistical analyses by calculating two extreme situations.
We took the 104 instances where both seedlings were
dead or where they were within 1 cm in height, and in
the first situation assigned the winner to be the initially
taller seedling, in the second situation we assigned the
initially shorter seedling to be the winner, then we carried
out goodness-of-fit tests, testing both sets of hypothetical
data against the expected distribution, in both cases
the statistic was very highly significant, P < 0.001. We
conclude from these tests that whatever the outcome of
the 104 trials it would not have changed our conclusions
that the results we obtained were very highly significantly
different from that expected from binomial distributions.
The outcome of interspecific competition trials where
the two seedlings were the same size to start with was
compared with the expectation from a binomial by a
goodness-of-fit test. We calculated the number of wins
for each species in a pair (values range from 0–10), and
from that calculated the deviations from an expectation
of 5 that would result if the seedlings were identical i.e. 3
wins and 7 wins both have a deviation of 2. We calculated
how many trials resulted in deviations of 0, 1, 2, 3, 4 and
5, we amalgamated those with deviations 3, 4, and 5,
because the expecteds were very small for 3, 4 and 5, and
then did a goodness-of-fit test between the observeds and
the expecteds calculated from a binomial distribution.
The outcome of the interspecific competition-trials
between large and small individuals was compared
with the expected distribution from two binomials. For
each axis in the Table (of the observed and expected
Competition among dipterocarps
321
Table 2. The outcomes of competition-trials between seedlings, the number of survivors, and mean (± SE) of height growth of 10 species of
Dipterocarpaceae. In competition-trials the winner was the tallest seedling if both survived, the survivor if one died, or if both were dead at the
final enumeration the tallest seedling at the last enumeration with a live seedling (hence wins can exceed survivors). The mean height growth over
22 mo was calculated as the mean of 9 or 10 interspecific competition-trials (each species competed against all other species with a replication of
10, so for example for D. lanceolata XY, 38.7 is the mean of 9 means: tall D. lanceolata vs. tall Hopea sp.; tall D. lanceolata vs. tall S. beccariana and so
on, for D. lanceolata Xy 47.0 is the mean of 10 means: tall D. lanceolata vs. short D. lanceolata; tall D. lanceolata vs. short Hopea sp.; tall D. lanceolata vs.
short S. beccariana and so on. X and Y signify tall seedlings, x and y short seedlings.
Competition-trials
XY
Wins
of X
Species
Dryobalanops lanceolata
Hopea sp.
Shorea beccariana
Shorea falciferoides
Shorea johorensis
Shorea leprosula
Shorea fallax
Shorea seminis
Parashorea malaanonan
Parashorea tomentella
Total
Mean of means
XY
Survivors
of X
(max. poss. 90)
36.5
21.5
33.5
36
49.5
77
34
36.5
63.5
62
78
72
54
81
71
76
62
77
71
80
722
(max. 900)
XY
Mean height
growth
(cm) of X
Xy
Wins
of X
Xy
Survivors
of X
Xy
Mean height
growth
(cm) of X
xY
Wins
of x
xY
Survivors
of x
xY
Mean height
growth
(cm) of x
(n = 9)
(max. poss. 100)
(n = 10)
(max. poss. 100)
(n = 10)
38.7 ± 0.5
27.4 ± 0.6
32.5 ± 0.6
36.1 ± 0.7
50.7 ± 0.7
86.3 ± 1.2
32.8 ± 0.8
34.9 ± 0.8
46.3 ± 0.5
51.3 ± 0.9
70
92
65
84
70
71
78
95
86
86
91.5
86
68.5
72
72.5
90
89
94
93.5
90
784
860
(max. 1000) (max. 1000)
47.0 ± 0.5
40.1 ± 0.4
41.6 ± 0.8
42.1 ± 0.4
56.3 ± 0.8
90.2 ± 0.8
37.0 ± 0.6
41.1 ± 0.5
53.9 ± 0.4
52.7 ± 0.6
11
85
13.5
82
18.5
58
8.5
82
22.5
46
46
74
9
44
18
91
32
77
37
79
216
718
(max. 1000) (max. 1000)
21.4 ± 0.7
21.5 ± 0.4
27.7 ± 0.8
21.7 ± 0.7
37.6 ± 1.2
67.0 ± 1.0
24.5 ± 2.0
21.4 ± 0.8
37.5 ± 0.8
40.7 ± 0.7
43.7 ± 5.4
50.2 ± 4.9
32.1 ± 4.6
distributions) the expected is a binomial and the expected
numbers in the cells were obtained by multiplying: the
expected value for that row, by the expected value for that
column, by 45 (the number of trials in this experiment).
The resulting ‘expecteds’ Table had very low values in
many of its peripheral cells, so cells were amalgamated
into nine final cells (and the observed values as well) to
allow a goodness-of-fit test of the data.
RESULTS
Survival
Of the original 2900 seedlings, 2300 survived for 22 mo
(79%). Survival was highest (86%) for large individuals
competing with small individuals (X in Xy competitiontrials); was 80% for X in XY competition-trials and 72%
for x in xY competition-trials (Table 2).
Growth
Seedlings that survived, grew on average by 42 cm in
22 mo (Table 2). The larger seedlings when pitted against
the smaller seedlings grew more (50 cm), the smaller
when pitted against the larger grew less (32 cm). There
were big differences between species (P < 0.001): in Xy
competition-trials S. leprosula grew 90 cm, when it was
taller (P < 0.001, for all nine comparison between S.
leprosula and the other species); S. johorensis grew 56 cm
(P < 0.001, for all nine comparison between S. johorensis
Figure 1. The relationship between growth of seedlings when they are
small (x in xY) and growth when they are large (X in Xy). The regression
equation is y = 0.892x + 12.7, r2 = 0.92, P < 0.001.
and the other species), the other eight species (when they
were taller) grew between 37 cm (S. fallax) and 46 cm (P.
malaanonan) and were mostly not significantly different
(Table 2).
Seedlings of species that grew faster than other species
in high light (15% above-canopy light) also grew faster
than other species in low light (when they were shorter
and shaded by taller seedlings), r2 = 0.90, P < 0.001
(Figure 1). The light beneath the canopy of the taller
seedlings was not low enough (it was not measured) to
suppress the growth of the smaller seedlings.
322
TANNER ET AL.
Table 3. The outcomes of interspecific competition between the 10 species of dipterocarp where the seedlings were initially the same size (the XY
experiment). The number in a cell shows the number of times out of 10 that the seedlings of the species in the row were taller (at the final recording)
than the species in the column, e.g. the cell for row Hopea sp. and column Shorea beccariana has 4 in it, thus of the 10 pots with initially equal-sized
Hopea sp. and S. beccariana, at the final recording Hopea sp. was taller that the S. beccariana 4 times (and S. beccariana taller than Hopea sp. 6 times).
The empty cells are ‘mirror image’ cells, which are not filled because it would mean plotting the same data twice (also we did not pit tall A against
tall A, and so on). The deviations from the expected value of 5 were highly significant (goodness-of-fit test P < 0.001 – after grouping deviations of
3, 4 and 5 because the expected (from a binomial distribution) were too small).
Dryobalanops lanceolata
Hopea sp.
Shorea beccariana
S. falciferoides
S. johorensis
S. leprosula
S. fallax
S. seminis
Parashorea malaanonan
Hopea
sp.
Shorea
beccariana
7
7
4
S. falciferoides
S. johorensis
S. leprosula
S. fallax
S. seminis
8
2
3
2
1
2
5
1
1
0
1
2
6
5
6
4
8
9
3
4
7
4
7
9
5
The pattern of height growth in Xy competition-trials
was usually that the taller seedling in a pair grew relatively
faster that the shorter seedling, thus the ratio of the
heights of the taller seedling to the smaller seedling
increased with time, of the 641 pots with two seedlings
alive in May 1999, which initially had dissimilar-sized
seedlings, 424 of the slopes were positive (significantly
more than expected from a standard normal distribution,
P < 0.01). A different analysis of the same data reinforce
the idea that usually the taller seedling grew more than the
shorter seedling – the absolute height difference between
the seedlings increased with time in 474 of the 641 plots.
Thus, we conclude that the pattern we have measured
would strengthen with time – the tall seedlings would
tend to become even taller than the shorter in about twothirds of the competition-trials.
The outcomes of competition-trials between species with
equal-sized seedlings
Overall the distribution was highly significantly different
from that expected by chance, because of the 45
interspecific competition trials there were 33 outcomes
where a species won 7, 8, 9 or 10 times out of ten
(χ 2 = 56.2, P < 0.001). Of these 33, 10 were for a
species winning 9 or 10 times out of 10, i.e. the species
acted as a dominant; they were: S. leprosula which won
7 of its 9 interspecific competitions, P. malaanonan 2,
and S. johorensis 1 (Table 3). Conversely there were
12 interspecific competition-trials where a species only
won either 4, 5 or 6 times out of 10, i.e. at or very
close to equality between the species.
The outcomes of competition-trials between species with
unequal-sized seedlings – ‘height dominance’ and ‘species
dominance’
The most frequent outcome of the competition-trials
between different species that were also a different
Parashorea
malaanonan
3
0
3
3
1
7
3
3
P. tomentella
0
2
4
2
2
7
4
2
5
size was that the initially taller seedling ‘won’ (won
means being either taller or the survivor after 22 mo).
When considering individual pots (1000 Xy competitiontrials) the larger seedling (X) won on 784 occasions,
of those the smaller seedling (y) had died in 282 cases
(Table 2); this pattern was highly significantly different
from the expected binomial distribution (χ 2 = 101,
P 0.005). The tendency to win when the competitor
was the smaller (xY competition-trials) was much less –
216 of 1000 competition-trials (Table 2). The tendency
to win when large is also a tendency to lose when
small (Figure 2) and thus ‘height dominance’, where
the outcome of competition-trials between two species,
which differed in size, was determined by the initial 10 cm
height difference. The opposite was ‘species dominance’
where the outcome of competition-trials between two
species was determined by the species difference, not
the initial 10 cm height difference. Of the 45 possible
outcomes from interspecific competition trials, 23 showed
‘height dominance’ and 6 ‘species dominance’ and
16 were unclear (Table 4); this was highly significantly different from expected binomial distributions
(Table 5).
Although the majority (23 of 45) outcomes of competition-trials between unequal-sized seedlings showed
‘height dominance’ about one eighth showed ‘species
dominance’, this resulted in the following trends across
species. If a particular species tended to win in Xy
competition-trials (X against all possible y) then it did
relatively well in xY competition-trials (x against all
possible Y, Figure 2, r2 = 0.93, P < 0.001), it also did
well in XY competitions (Table 2, r2 = 0.92, P < 0.001).
Three species dominated in some competition-trials
(Table 6). They were: Shorea leprosula (4 of 9 interspecific
competition-trials); S. johorensis (1/9) and P. tomentella
(1/9). But even these ‘species dominants’ did not dominate
all species; they had ‘height dominance’ relationships in
many interspecific competition-trials.
Competition among dipterocarps
323
Figure 2. The number of wins (out of 100) for each species after unequal-sized competition against all species (including itself); x-axis when it was
the larger seedling, y-axis when it was the smaller seedling: each point represents one species. The identity of the species is shown by the first letter of
the genus and the first letter of the species (e.g. Sl = Shorea leprosula) except So = Shorea fallax. The size-effect axis shows where the points would lie if
the size of the individuals was the only factor determining the outcome (e.g. if the tallest seedling always won then all species would have an x-axis
score of 100 and a y-axis score of 0). The species-effect axis shows where the point would lie if the identity of species was the only factor determining
the outcome (e.g. if a species dominated all but one interspecific competitions, its x-axis score would be 90 and its y axis score 90). The actual data
show strong effects of differences in initial height and weaker but significant differences between species.
Leaf attributes
Leaf [N] was quite low (about 15 mg g−1 ) and only
varied amongst species by 5 mg g−1 (Table 1). Specific
leaf area averaged about 130 cm2 g−1 and ranged from
103–167 cm2 g−1 . Leaf thicknesses ranged from 73 µm
in Shorea fallax to 175 µm in Dryobalanops lanceolata, with
only D. lanceolata being significantly thicker than the other
species.
DISCUSSION
Winners and losers or ecological similarity?
There are several reasons for thinking that many of
the species we studied are ecologically similar. Firstly
when grown in standard conditions the height growth
of tall seedlings (when pitted against tall seedlings of
all other species) did not differ significantly between
species for eight of ten species. The exceptions were S.
leprosula, which grew taller than all other species and
S. johorensis, which was taller than all but S. leprosula,
P. malaanonan and P. tomentella. Secondly, when larger
seedlings were pitted against smaller the larger usually
won (784 wins out of 1000). Thus in 23 of 45
competition-trials between species, where seedlings also
differed in height, the height of the original seedlings
dominated the outcome, taller X beat shorter y, but taller
Y beat shorter x. Our findings broadly agree with the
other studies of dipterocarps where growth of seedlings
of different species was compared (there seem only to be
studies of growth – there are no studies of actual competition between seedlings); though the authors of those
studies usually drew attention to differences between
groups of species, we draw attention to the many
similarities between individual species. Three studies
exhibit these similarities. In the first Sasaki & Mori (1981)
showed equal seedling height in Vatica odorata, Hopea
helferi and Shorea talua after 1 y at a given diffuse light
intensity. In the second study, Still (1996) gave results
for the growth of eight species and while no statistical
analyses by species was done, it is clear from her figure
13.8 that there are two groups of species where growth
324
TANNER ET AL.
Table 4. The observed and expected distributions for the outcomes of competition between taller and shorter individuals of the ten species in all
combinations; N = 45 combinations. Values are the number of species pairs, of 45, which show the particular combination of wins; values of 0.5
arise from the fact that there is no reason to plot a particular result e.g. X in Xy = 1, Y in xY = 10, rather than X in Xy = 10, Y in xY = 1, so 0.5 is
plotted in each. Numbers in bold show ‘height dominance’ (for definition see Results), numbers in italics show ‘species dominance’; the expecteds
were calculated from binomial distributions – see Methods.
Wins when Y is taller
initially (Y in xY)
Wins when X is taller initially (X in Xy)
0
1
2
3
4
5
6
7
8
9
0.5
1.0
0.5
0.5
0.5
0.5
1.0
1.0
2.5
1.5
0.5
2.0
1.5
1.0
2.0
3.0
1.0
1.0
0.5
1.0
0.5
2.0
3.0
1.5
1.5
1.0
0.5
1.0
0.5
10
Observed
10
9
8
7
6
5
4
3
2
1
0
10
9
8
7
6
5
4
3
2
1
0
0.5
0.5
0.5
0.5
2.0
2.0
2.5
0.5
0.5
0.5
0.5
Expected
0.00
0.00
0.00
0.01
0.01
0.01
0.01
0.01
0.00
0.00
0.00
0.00
0.00
0.02
0.05
0.09
0.11
0.09
0.05
0.02
0.00
0.00
0.00
0.02
0.09
0.23
0.41
0.50
0.41
0.23
0.09
0.02
0.00
0.01
0.05
0.23
0.62
1.08
1.32
1.08
0.62
0.23
0.05
0.01
rates were not different (group 1, S. leprosula, S. parvifolia
and S. johorensis; and group 2, Vatica sarawakensis,
S. paucifolia and S. fallax). Finally, the third study by
Gunatilleke et al. (1997) showed that of eight species
of dipterocarp six were similar in height after 24 mo
of growth in standardized conditions; the means per
species ranged from 25.3–45.7 cm, with six in the range
25.3–34.5 cm – many of these species are unlikely to
be significantly different (though tests were not done).
Thus, we conclude that many species are not significantly
different when careful quantitative comparisons of
growth are made in standardized conditions and thus
they can be regarded as ecologically similar, in terms of
growth.
In contrast to the ecological similarity of most of our
species (and other species studied by other researchers),
three of our ten species showed some dominance (6 of
45 possible interspecific interactions), these were all light
hardwood species, whose seedlings grew fastest in our
experiment (t-test of growth of X in XY competitiontrials, three species that showed some dominance cf.
seven that did not, P = 0.05) – this is not surprising
because taller seedlings were deemed winners. Even
these three species were not always ‘dominant’ but had
‘height dominance’ relationships in some interspecific
and intersize competitions, especially those with other
0.01
0.09
0.41
1.08
1.89
2.31
1.89
1.08
0.41
0.09
0.01
0.01
0.11
0.50
1.32
2.31
2.81
2.31
1.32
0.50
0.11
0.01
0.01
0.09
0.41
1.08
1.89
2.31
1.89
1.08
0.41
0.09
0.01
0.01
0.05
0.23
0.62
1.08
1.32
1.08
0.62
0.23
0.05
0.01
0.00
0.02
0.09
0.23
0.41
0.50
0.41
0.23
0.09
0.02
0.00
0.00
0.00
0.02
0.05
0.09
0.11
0.09
0.05
0.02
0.00
0.00
0.00
0.00
0.00
0.01
0.01
0.01
0.01
0.01
0.00
0.00
0.00
Table 5. The observed and expected values for the outcomes of
competition between taller and shorter individuals of the ten species
(calculated from Table 4) and Chi-square for the goodness-of-fit test.
Number of wins
Expected numbers of 45
7–10
4–6
0–3
Observed numbers of 45
7–10
4–6
0–3
Chi-square (total = 391)
7–10
4–6
0–3
0–3
4–6
1.32
5.09
1.32
5.09
19.6
5.09
3
0
0
2.13
5.1
1.3
7–10
1.32
5.09
1.32
7.5
1
0
23
7.5
3
1.1
17.7
5.1
355.2
1.1
2.1
light hardwoods. But also, interestingly, one (S. leprosula)
showed ‘height dominance’ with the heavy hardwood
Hopea sp. (Table 6) i.e. Hopea sp. outcompeted S. leprosula
when Hopea sp. was 10 cm taller initially and vice
versa. Our results showing differences between species
are also in agreement with three other studies. Firstly,
Still (1996) showed that seedlings of two of the species
we studied had relatively high growth and mortality
rates in natural populations in the shaded understorey
(in contrast to our light levels which were like those
unclear
Height dominates
Height dominates
Height dominates
Height dominates
Height dominates
S. leprosula dominates S. leprosula dominates
unclear
unclear
unclear
unclear
Height
dominates
unclear
unclear
Height dominates
Height dominates
unclear
325
found in gaps) in nearby forests. Secondly, Whitmore &
Brown’s (1996) experimental gap study of Hopea nervosa
and Shorea johorensis, showed that after 40 mo H. nervosa
seedlings from the original seedling bank were taller
than S. johorensis but after 53 mo the S. johorensis
were taller. Our competition trials showed that Shorea
johorensis dominated when in competition with Hopea
sp. i.e. that size differences were less important than
species differences in competition-trials between these
two species. Thirdly, Zipperlen & Press (1996) compared
S. leprosula with Dryobalanops lanceolata, species from
different wood-density groups, and found more growth,
in gaps, in S. leprosula – the species with lower wood
density; as we found when S. leprosula grew more than
D. lanceolata.
Overall, we interpret the results to show that many
species are ecologically similar but a few will dominate a
few others (these are species which have higher growth
rates in gap light conditions); similarity and dominance
depend on which species are competing.
Growth rate in high light versus low light,
and growth and survival
S. seminis
Parashorea
malaanonan
unclear
Height dominates
P. tomentella dominates
unclear
Height dominates
Height dominates
Height dominates
Height dominates
S. leprosula dominates Height dominates
unclear
unclear
unclear
unclear
Height dominates
S. leprosula dominates Height dominates
Dryobalanops Height
Height
Height dominates unclear
lanceolata
dominates
dominates
Hopea sp.
unclear
Height dominates S. johorensis dominates
Shorea
Height dominates Height dominates
beccariana
S. falciferoides
Height dominates
S. johorensis
S. leprosula
S. fallax
P. tomentella
Parashorea
malaanonan
S. seminis
S. fallax
S. leprosula
S. johorensis
S. falciferoides
Shorea
beccariana
Hopea sp.
Table 6. The ‘height dominance’ or ‘species dominance’ relationships (for definition see Results) between the 10 dipterocarp species based on the outcomes of interspecific and intersize competition
(the Xy experiment); of the 45 possible comparisons (Ab and aB are, for example, one comparison), 23 show ‘height dominance’, 6 ‘species dominance’ and 16 are unclear.
Competition among dipterocarps
We found that species that grew fastest, relative to other
species, in high light when they were tall (X in Xy) also
grew faster, relative to other species that were similarly
shaded, when they were small (x in xY, Figure 1); the
light levels under the shade of taller seedlings were not
low enough to stop growth. There are few other data
for dipterocarps with which to compare our results,
but Ashton (1995) gives results for seedlings of four
dipterocarps growing in shade houses where light was
carefully measured; using his data we compared growth of
seedlings in ‘dark understorey light’ to growth in the best
light environment (usually not full sunlight) and found a
trend where the species that grew best in high light grew
least well in low light (r2 = 0.71, P = 0.15, not significant
but probably because there were too few species) – an
opposite pattern to ours. Studies of growth of seedlings of
tropical trees other than dipterocarps have shown a range
of patterns of rank order of seedling growth when many
species are compared. Most of these studies show that
species which grow fast in gap light grow more slowly
than other species in understorey light (Sack & Grubb
2001) i.e. opposite to our findings; it is likely that the light
levels above our shorter seedlings was not low enough
to cause the normal reversal of the rank order of species
growth rates.
There was no relationship between growth in high
light and survival in low light (r2 = 0.00, Figure 3), thus
we found no support for the classical paradigm, which
is that species that can grow fast in high light have
high respiration rates, which they cannot gear down
326
Figure 3. The relationship between survival of seedlings (number of
survivors of 100 initially) when they are small (x in xY) and growth when
they are large (X in Xy). The regression equation is y = 0.0235x + 70.6,
r2 < 0.01, P = 0.95.
sufficiently to survive for long in low light. Our smaller
seedlings were probably not shaded enough to cause
enough of them to die; though our mortality was 28%
over 22 mo for the initially smaller seedlings.
TANNER ET AL.
with bigger seeds would give taller seedlings. Analysis of
data on dipterocarp seedling and nut sizes, published by
others, also shows no relationship between nut sizes and
seedling sizes. For example for the eight species studied by
Gunatilleke et al. (1997) there was no correlation between
nut size (from Ashton 1980) and height of control
seedlings after 24 mo; nor was there any correlation
between nut size and seedling height for five species in
the understorey studied by Fox (1973) or for seedlings of
three species grown in dark understorey light by Ashton
(1995). These findings raise the question of why some
dipterocarp species have big seeds if it is not to make tall
seedlings? It is not to make more roots because in the
eight species studied by Gunatilleke et al. (1997) there was
no correlation between nut sizes and root mass ratios –
though these were for 24-mo-old seedlings that had been
growing in 50% full daylight and might have outgrown
any effect of nut size. Perhaps larger-seeded species have
higher rates of survival in the low light of understoreys?
Published studies of mortality from field plots (e.g.
Delissio et al. 2002), which distinguish new recruits from
older seedlings, have too few dipterocarps to test this
hypothesis.
How relevant is the experiment to field conditions?
Correlates between species characteristics
We measured leaf nitrogen per mass and specific leaf
area as important measures related to the physiology of
different species. The importance of these measures was
demonstrated by a worldwide study of leaf traits where
three traits: rate of photosynthesis per mass; specific leaf
area; and nitrogen per mass (of six studied) accounted for
82% of the variation in a worldwide data set (Wright
et al. 2004). In our study leaf nitrogen concentration
and SLA were not correlated with each other; we had
expected that [N] per mass and SLA would be positively
correlated (cf. Reich et al. 1999) nor did they correlate
with growth, nor were they significantly different between
wood-density classes (light hardwoods cf. medium plus
heavy hardwoods). Barker et al. (1997) also reported
no relationship between photosynthetic rates and wood
density. Thus, it seems that there is not a simple suite
of characteristics, or even a quantitative trend; seedlings
of these species are very similar, the few differences that
did exist were not correlated with anything we measured
(e.g. we expected that the faster growth of Shorea leprosula
would be associated with high leaf nitrogen concentration
and high specific leaf area).
Seedlings of different species were of similar height
(about 30 cm) to start with, despite the fact that nut
volume of nine species for which we have data ranged
from 1–31 cm3 (Table 1). We expected that bigger nuts
The experimental results show that when seedlings of
different species and different heights are pitted against
one another the height rather than the species often
determines which individual is the tallest after 22 mo.
How likely are such scenarios in gaps in the forest? To
answer this question data are needed on the exact position
of seedlings relative to each other, and of their growth and
mortality. There seems to be little if anything published,
which specifically combines data on the growth of seedling
and the size, identity and distance to nearest neighbours,
for seedlings in gaps or in light conditions similar to that
found in such gaps. Such data are necessary to investigate
the importance of size differences in competition; it is likely
that the field data from some seedling studies have the
necessary information.
To what extent are tree species of tropical rain
forests similar?
One of the striking findings of our experiment was the
similarity of seedlings of many species of dipterocarp.
Our experiment was well designed to assess inherent
differences between species because the seedlings were
grown in very similar conditions: homogenized soil in
same-sized pots; equal watering; and equal light (at least
for the taller seedlings in each pot).
Competition among dipterocarps
The lack of a correlated suite of differences between
seedlings of these species is consistent with the finding
that the outcome of competition-trials between species
is dominated by the relative heights of the competing
individuals; in a nutshell, many of these species are
indistinguishable ecologically – they are functionally
similar in terms of their response to the physical environment. Thus natural selection does not have distinct phenotypes to act upon, many of the species are ecologically
similar and unlikely to be eliminated, due to their
species characteristics, when seedlings of dipterocarps
compete; this will tend to allow the persistence of high
diversity in these species-rich rain forests of SouthEast Asia.
We wonder to what extent other groups of canopy
tree species in other tropical forests are similar, especially
species within the same family, or closely related families?
There have been many comparisons of species grown
in similar environments (summarized in Turner 2001);
while the authors usually point out the differences
between species or groups of species, we wish to point
out the similarities of many species. Whether species are
similar or different may be reliably indicated by their
height growth relative to other species when they are not
competing, because in our study those that grew faster
were also more likely to win interspecific competitiontrials (i.e. they were not ecologically similar). It would
be informative now to study pairwise competition of the
common species in other tropical forests, especially in
forest gaps as well as in a shade-house; such experiments
should include treatments which investigate how close
individuals have to be to compete with each other. It is
likely that the larger the difference in height of competing
seedlings the more likely the taller one is to win. Similarly
the greater the distance between competing seedlings the
greater the height difference needs to be for the taller
seedling to win the competition to fill a canopy gap.
Experiments in the forest would test whether the strong
advantage of a 10-cm height difference, which we have
measured in a shade house with gap light levels, is seen
in real forest gaps.
327
Cambridge provided additional funding to V. K. T. and
The Royal Society funded E. V. J. T. The Danum Valley
Management Committee granted permission for the work
to be carried out. Three anonymous reviewers made very
helpful suggestions.
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