Canopy Closure and The Distribution of Tropical Forest Tree Species at La Selva, Costa Rica

Canopy Closure and the Distribution of Tropical Forest Tree Species at La Selva, Costa Rica
Author(s): Milton Lieberman, Diana Lieberman, Rodolfo Peralta and Gary S. Hartshorn
Source: Journal of Tropical Ecology, Vol. 11, No. 2 (May, 1995), pp. 161-177
Published by: Cambridge University Press
Stable URL: http://www.jstor.org/stable/2560103
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Journal of Tropical Ecology (1995) 11:161-1 78.
Canopy closure and the distribution of tropical

forest tree species at La Selva, Costa Rica
MILTON LIEBERMAN,* DIANA LIEBERMAN,*

RODOLFO PERALTA,t and GARY S. HARTSHORN+
*Department of Biology, University of North Dakota, Grand Forks, ND 58202-9019,

USA, and Apartado 35, Santa Elena de Monteverde, Puntarenas, Costa Rica
t Centro Cientifico Tropical, Apartado 8-3870, and PORTICO, S.A, San Jose, Costa
Rica
+ World Wildlife Fund, 1250 24th St., NW, Washington, DC 20037, USA
ABSTRACT. An index of canopy closure was used to estimate closure above the crowns of all
trees B 10 cm dbh in 1 1.11 ha of undisturbed lowland tropical forest at La Selva, Costa Rica. To
correct for the effects of tree size on canopy closure, we used the residual of the regression of the
canopy closure index on tree size. Analyses were carried out for the 104 species which had B6
individuals; a total of 3224 trees were included. Nine species were found to have their crowns in
significantly more open conditions than expected by chance and five species were found to have
their crowns in significantly more closed conditions than expected by chance (P < 0.05). The
remaining 90 species (86.5% of the assemblage) were distributed at random with respect to canopy
closure, occupying the available light conditions indiscriminately. Species occurring under higher
light levels did not show a narrower range of tolerance than did other species. Most species were
found to occur over a substantial proportion of the canopy closure continuum present in the stand;
overlap among the great majority of species in the assemblage is extensive. The results support
the view that tropical forests comprise assemblages of generalist tree species, and raise questions
about the classic notions of gap-phase dynamics.
KEY WORDS: canopy closure, Costa Rica, forest structure, gaps, habitat preference, La Selva,
light, niche breadth, shade tolerance, tropical forest.
INTRODUCTION
The dynamic processes of tropical primary forests produce over time a structure
of great heterogeneity. Stem density, basal area, tree height and canopy thick-
ness vary over short distances (Hartshorn 1978, 1980, Lieberman et al. 1985b,
Lieberman & Lieberman 1994, Richards 1952, Whitmore 1978, 1989). Canopies
range from one to several tree crowns in depth, and are riddled with openings
that range in size from a few square decimetres to a hectare or more (Hartshorn
1980, Johns 1986, Martinez-Ramos 1985, Popma et al. 1988, Sanford et al.
1986, Uhl et al. 1988, Whitmore 1974, Yih et al. 1991). This three-dimensional
structural complexity gives rise to wide variation and heterogeneity in forest
161
162 MILTON LIEBERMAN ET AL.
light environments (Bjorkman & Ludlow 1972, Chazdon & Fetcher 1984a,b,
Rich et al., in press).
The response of tree species to this variation has been presumed to be import-
ant for the maintenance of the high species diversity that characterizes tropical
forests, permitting coexistence through diversification and separation of light
niches among species in the assemblage (Denslow 1980, 1987, Orians 1982).
Treefall gaps represent one extreme of the range of light conditions, and the
overwhelming majority of studies concerning species distributions in forest light
environments are conceived as comparisons between gaps and the surrounding
forest (Brokaw 1985, 1987, Denslow et al. 1990, De Steven 1988, Fisher et al.
1991, Hubbell & Foster 1986a, Kennedy & Swaine 1992, Raich & Gong 1990,
and maniy others; see reviews in Denslow 1987, Denslow & Hartshorn 1994).
Although gaps are of interest in their own right, we have suggested
(Lieberman et al. 1989, Lieberman & Lieberman 1991) that the perception of
the surrounding forest as a comparatively homogeneous standard against which
gaps can be compared may be frankly unwarranted. We argue that the dicho-
tomy of forest environments into gap and non-gap conditions is both unrealistic
and difficult to implement with rigour and consistency, and that forest light
environments should be treated as a continuum.
Previous work has largely neglected the light environment of the forest as a
whole, and there is little information on the distribution of light levels available
to forest trees. Consequently, we do not know whether tree species are distrib-
uted preferentially with regard to light conditions. We know next to nothing of
the breadth or specificity of species distribution patterns, nor the extent to which
tree species within an assemblage overlap in their use of the light environment.
In this paper we treat the light environment as a continuum, using an index
of canopy closure (Lieberman et al. 1989) to assess the light environment at the
crown of each tree B10 cm dbh in an undisturbed lowland tropical forest; we
test whether species show preference with regard to light conditions; and we
explore the degree of separation and overlap of species with respect to available
light conditions.
STUDY SITE
The study was carried out at La Selva Biological Station (100 26' N,
830 59' W) in the Caribbean lowlands of Costa Rica. Mean annual rainfall
is around 4000 mm. Details of the area are reported elsewhere (Hartshorn 1983,
Lieberman et al. 1985a,b,c, 1990, Lieberman & Lieberman 1987, 1994).
Data were collected in three permanent inventory plots totalling 12.4 ha in
area. The plots range in elevation from 32 to 71 m, and bear primary tropical
wet forest. The canopy is uneven and generally less than 40 m high, although
some trees reach 50 m. Mean density of stems 10 cm dbh is 446-ha-', and
mean species richness is 95.5 species ha-'. The forest is very dynamic; annual
Canopy closure and tree distribution 163
mortality of individuals 310 cm dbh is from 2.03 to 2.34% y-', producing a

stand half-life of 30-34 years. Mortality and recruitment are in steady state.
Regular inventories have been conducted in the permanent plots since their
establishment in 1969-1970. All stems ? 10 cm dbh are tagged, mapped to the
nearest metre, measured and identified. Information used in this study was
collected in 1989.
The La Selva study area exhibits the wide variation in forest structure that
is characteristic of undisturbed tropical forests (Lieberman et al. 1989, Lieber-
man & Lieberman 1991, 1994, and unpublished data). Only 6.3% of the area
is gaps, but fully 21 % of the gap area is made up of large gaps >400 m2
(Sanford et al. 1986). The frequency distribution of gap sizes at La Selva appears
unremarkable in comparison with other forests (Denslow & Hartshorn 1994).
METHODS
The index of canopy closure, G, is an estimate of shading at a given site based

upon the density and heights of neighbouring trees (Lieberman et al. 1989,
Lieberman & Lieberman 1991). The index may be calculated for any point in
the three-dimensional space of the forest using the location and size of trees
within mapped forest plots. Variation in light availability, over both horizontal
and vertical dimensions, can be considered. In this study, closure was measured
at the top of the crown of each tree of interest.
The index (Figure 1) uses the following measures: the horizontal distance (d)
between the focal tree and each taller neighbour within a 10 m radius; and the
height of difference (A ht) between the focal tree and each taller neighbour.
From these two values, we compute the distance from the top of the crown of
the focal tree to the top of the crown of each taller neighbour (the hypotenuse,
h). The ratio A ht/h is the sine of the included angle 0. The index of canopy
closure is defined as the sum of these ratios for all taller neighbours within the
specified radius:
G = sin 0
i=1
Tree height was estimated allometrically using the empirical relation

(independent of species)
Height = 5.5 dbh 3
The canopy closure index thus defined provides an estimate of shading above
the crown of a given focal tree.
The analysis and interpretation of canopy closure values for a set of focal
trees must take into account the size of the focal trees themselves. Forests
characteristically display strong vertical light gradients; by virtue of size alone,
the crowns of small understorey trees tend to occur in shadier environments
Figure 1. Diagrammatic representation of the canopy closure index G. The index is calculated for the top
of the focal tree (shaded crown), using the distance (d) and height difference (A ht) between the focal tree
and all taller neighbours. The ratio of the height difference to the hypotenuse h is the sine of the angle 0.
The index G is defined as the sum of the sines of the angle 0 between the focal tree and all taller neighbours
within a 10-rn radius.
than the crowns of large canopy trees. To compare closure values between
species, one must first remove the effect of tree size on the index.
There is a linear relationship (Figure 2) between the closure index and the
reciprocal of dbh (r = 0.82 1, 4391 df; P < 0.00 1); all trees of all species were
used. The reciprocal of tree size has been used because the untransformed
relationship is hyperbolic. The transformation linearizes the relationship and
reverses the order of tree sizes along the abscissa; points representing the largest
trees are nearest the origin.
The regression represents the mean vertical gradient in canopy closure in the
stand. The residual from each point to the regression line was calculated. Points
above the regression line (positive residuals) represent individual trees found
in shadier conditions than would be expected on average for their size; those
below the line (negative residuals) represent trees in lighter conditions than
would be expected on average for their size. The closure index reflects the actual
20 -
x 105
CD
G-Lj
2 4 6 8 10
1000 / DBH (mm)

Figure 2. Relationship between the canopy closure index and tree size for all trees ? 10 cm dbh. Tree size
has been transformed (1 000/dbh) to linearize the distribution; small trees (10 cm dbh) are at the right-hand
side of the graph. The largest tree in the sample is 230 cm in diameter. High closure values indicate shady
conditions: low closure values indicate high light levels, a value of 0 representing exposure to full sunlight.
The regression reflects the mean expected canopy closure for trees of a given size.
level of shading to which a tree is exposed; the residual of the canopy closure
index is the closure index corrected for tree size.
We calculated canopy closure at the top of the crown of each tree B 10 cm
dbh in the three La Selva permanent plots. Such trees at La Selva range in
height from c. 10-45 m, representing nearly 80% of the three-dimensional
volume of the forest. As we excluded a 10 m wide buffer zone around the margin
of each plot, the total area studied was 11.11 hectares. Altogether 4392 trees
were included in the study. Palms, lianas and tree ferns were omitted because
of their unusual growth form and allometry. Particular attention was given to
the 104 species that had six or more individuals (N = 3224).
The canopy closure index for individual trees (N = 4392) varied from 0 (for
canopy trees with no taller neighbours within a 10 m radius) to 14.93 (for small
trees in the deepest shade of the understorey) . The mean closure was 4.05 (?SE
600 -
500-
:D 400-
Z 00 3
fl? 200-
w
m
z 100
0 ?
0 5 1 0 1 5 20
CANOPY CLOSURE INDEX G
Figure 3. Frequency distribution of canopy closure values for all trees ? 10 cm dbh. The distribution is
positively skewed; most trees, because of the location and height of their crowns, are found in moderate to
high light levels.
0.054). The frequency distribution of canopy closure values for individual trees
is skewed to the right (Figure 3). Comparatively few individuals B 10 cm dbh
are found to have their crowns in the shadiest conditions; this is, of course,
influenced by the height class distribution of trees in the stand.
Residuals of the closure index (Figure 4) form a symmetrical distribution
centred near zero which ranges from -4.727 to 5.372. The mean residual was
0.000003 (?SE 0.021).
Residuals were sorted according to species. Species-level analyses were
limited to the 104 species represented by six or more individuals (N = 3224).
For each species we calculated the mean residual. The means ranged from
-1.153 to 1.111; the mean of the means was -0.0904 (?SE 0.4106). The
frequency distribution of mean closure by species is uneven, but roughly sym-
metrical (Figure 5); most species have their centre of distribution (corrected for
size) in environments of intermediate closure.
In order to assess canopy closure of each species in relation to that of other
trees in the stand, we compared the residuals of each species with the residuals
of the population of trees in general, using a Student's t-test.
Table 1 presents the results of the analysis, with species ranked according to
the value of Student's t. Of the 104 species tested, nine occur in significantly
500 -
V) 400-
> 300
z
Z
200
wX 0
m
Z 1000
0~~~~~~~
-6 -4 -2 0 2 4 6
RESIDUAL OF CANOPY CLOSURE

Figure 4. Frequency distribution of the residual of canopy closure for all trees > 10 cm dbh.
higher light levels than would be expected by chance, and five in significantly
shadier conditions than would be expected by chance (P < 0.05). The null
hypothesis was rejected for a total of 14 species, or 13.5% of those tested;
in multiple tests of this kind, one would expect to see around 5.2 spurious
rejections.
The remaining 90 species, or 86.5% of those studied, are distributed at
random with respect to present canopy closure levels in the stand, occupying
the available light conditions indiscriminately.
How are tree species within an assemblage distributed in relation to the light
environment? Residual values of trees in each species ranked according to Student's
t are shown in Figure 6. Species found in low light conditions are shown at the
top, and those in high light conditions at the bottom. Species form a continuum
in their distribution along a canopy closure axis. One sees neither discontinuities
nor discrete species groupings with respect to the light environment.
To what extent do tree species overlap in their use of the light environment?
It is apparent from Figure 6 that most species occupy a large proportion of the
available range of conditions. There is extensive overlap, rather than separation,
of species along a canopy closure axis. Within the context of the light environ-
ment of this forest stand, we see no evidence of strong niche separation among
tree species.
30 -
U)
o 20 -
0?
mn 10
0-_T
-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5
Figure 5. Frequency distribution of the mean residual of canopy closure for the 104 most abundant tree
species in the study area.
On the basis of growth rates, maximum diameters and projected lifespan,

the 46 most abundant species in the study plots were divided into four groups
(Lieberman et al. 1985a): (1) understorey species; (2) subcanopy species; (3)
long-lived canopy species; and (4) short-lived, fast-growing canopy and subcan-
opy species. Based on their growth behaviour and demography, the species in
Group 4 were hypothesized to be shade-intolerant.
Figure 7a-d displays the relationship between closure and diameter for indi-
viduals in each of these four species groups. Understorey trees (Figure 7a)
occupy a broad range of conditions when small. Few individuals exceed 20 cm
dbh, and not even the largest have their crowns in full sunlight. Subcanopy
trees (Figure 7b), when small, occupy the same range of light conditions as do
understorey species, but the crowns of larger individuals may encounter full
sunlight (G = 0). Long-lived canopy species (Figure 7c) are the most numer-
ous. As small trees they too are found in a wide range of light conditions. The
largest individuals of this group form the upper surface of the forest's canopy
structure and face the unobstructed sky. Fast-growing, short-lived species
(Figure 7d) are found within the same range of light conditions as the other
three species groups, although fewer have their crowns in deep shade. The
Table 1. Distribution of tree species with regard to canopy closure in primary tropical forest at La Selva,
Costa Rica. All species with >6 individuals are included. The residuals of canopy closure with respect to
tree size of each species were compared with the residuals of the population of trees in general using a t-test.
Mean canopy closure, mean residual, sample size and Student's t value are shown for each species; species
are ranked according to t. Negative residuals indicate occurrence under open condtions; positive residuals
indicate occurrence under closed conditions. ***, P < 0.001; * P < 0.01; *, P < 0.05. Species determina-
tions were carried out by R. Peralta and G. S. Hartshorn.
Closure
index
Species G Residual N t
1 Hampea appendiculata 1.188 -0.858 17 -2.960**

2 Cecropia obtusifolia' 0.499 -0.933 13 -2.818**
3 Adelia triloba 1.110 -1.153 8 -2.730**
4 Lonchocarpus oliganthus 3.279 -0.964 11 -2.671**
5 Inga thibaudiana 0.959 -0.546 30 -2.500*
6Pterocarpus rohrii 0.921 -0.510 34 -2.486*
7 Colubrina spinosa 1.858 -0.503 32 -2.370*
8 Guarea rhopalocarpa 1.215 -0.467 34 -2.274*
9 Inga pezizifera' 0.519 -0.685 12 -1.988*
10 Inga sapindoides 0.462 -0.703 10 -1.862
11 Psychotria grandistipula 1.133 -0.846 6 -1.736
12 Myrcia sp. upland 1.074 -0.769 7 -1.704
13 Otoba novogranatensis' 2.389 -0.410 21 -1.566
14 Ficus glaucescens 2.595 -0.685 7 -1.517
15 Lonchoca7pus velutinus 3.766 -0.544 10 -1.464
16 Cordia bicolor 1.349 -0.477 11 -1.324
17 Goethalsia meiantha' 0.775 -0.178 65 -1.195
18 Pleuranthodendron lindenii 0.750 -0.582 6 -1.194
19 Unonopsis pittieri 1.262 -0.428 11 -1.189
20 Jacaratia dolichaula 1.393 -0.499 8 -1.181
21 Laetia procera 0.740 -0.209 41 -1.120
22 Cecropia insignis 1.563 -0.441 9 -1.107
23 Guarea sp. 1.942 -0.437 9 -1.098
24 Inga sp. densifora H&P 1.033 -0.478 7 -1.060
25 Casearia arboreal 1.662 -0.159 62 -1.037
26 Carapa nicaraguensis 1.731 -0.175 47 -1.000
27 Eugenia sp. 1.643 -0.409 8 -0.968
28 Theobroma mammosum 2.849 -0.400 8 -0.947
29 Rauvolfia purpurascens 0.907 -0.179 26 -0.762
30 Simarouba amara 0.593 -0.216 16 -0.723
31 Hernandia didymanthera' 0.785 -0.147 30 -0.675
32 Virola koschnyi 1.094 -0.168 21 -0.642
33 Vochysia ferruginea 1.085 -0.269 8 -0.636
34 Guarea bullata 2.848 -0.112 42 -0.600
35 Apeiba membranacea 0.814 -0.122 33 -0.583
36 Veconcibea pleiostemona 0.877 -0.150 11 -0.416
37 Guatteria aeruginosa 0.779 -0.115 15 -0.373
38 Anaxagorea crassipetala 1.762 -0.074 33 -0.354
39 Inga umbellifera 0.821 -0.140 9 -0.352
40 Quararibea bracteolosa 1.724 -0.065 25 -0.273
41 Heisteria concinna 2.663 -0.095 10 -0.252
42 Inga coruscans' 1.125 -0.057 18 -0.202
43 Pouteria standleyana 2.255 -0.049 16 -0.164
44 Pouroua minor 1.624 -0.040 22 -0.157
45 Protium pittieri 1.163 -0.018 110 -0.152
46 Inga longispica 0.533 -0.040 18 -0.142
47 Naucleopsis naga 1.238 -0.019 57 -0.120
48 Dussia macroprophyllata 0.690 0.005 22 0.020
49 Miconia multispicata 0.520 0.008 13 0.023
50 Stryplhnodendron excelsum' 0.747 0.013 13 0.038
Table 1. Continued
Closure
index
Species G Residual N t
51 Pouteria neglecta 2.144 0.014 19 0.051

52 Parathesis chrysophylla 2.043 0.026 8 0.060
53 Trichilia moritzii 2.380 0.017 20 0.062
54 Rinorea deflexifora 1.749 0.013 39 0.065
55 Rheedia edulis 2.385 0.019 29 0.086
56 Ilex skutchii 0.437 0.041 8 0.097
57 Saccoglottis trichogyna 0.729 0.046 7 0.101
58 Ormosia sp. 1.191 0.050 8 0.118
59 Tapirira guianensis 1.658 0.048 9 0.120
60 Sloanea faginea 1.515 0.089 6 0.182
61 Protium glabrum 1.367 0.056 20 0.208
62 Cordia dwyeri 1.782 0.074 13 0.222
63 Pourouma aspera 1.462 0.039 49 0.224
64 Dendropanax arboreus 1.099 0.054 64 0.359
65 Guatteria diospyroides 1.702 0.115 16 0.386
66 Byrsonima crispa 0.980 0.182 7 0.404
67 Dipteryx panamensis 0.296 0.195 7 0.433
68 Brosimum lactescens 1.223 0.136 19 0.496
69 Coussarea taurina 3.019 0.232 7 0.513
70 Cupania livida 2.993 0.184 13 0.554
71 Pentaclethra macroloba 0.808 0.031 565 0.588
72 Warscewiczia coccinea 1.642 0.080 129 0.742
73 Andira inermis 1.662 0.223 16 0.746
74 AMlinquartia guianensis 1.063 0.232 15 0.752
75 Cespedesia macrophylla 0.482 0.226 16 0.757
76 Cassipourea elliptica 2.475 0.158 34 0.763
77 Terminalia amazonia 1.215 0.329 8 0.778
78 Inga densiNfora 2.344 0.291 11 0.807
79 Pouteria unilocularis 2.765 0.334 9 0.838
80 Pithecellobium elegans 1.329 0.276 14 0.864
81 Pouteria congestifolia 2.767 0.428 6 0.878
82 Chrysophyllum venezuelanese 1.691 0.324 11 0.899
83 Pterocarpus officinalis 0.641 0.240 22 0.941
84 Sclerolobium sp. 4.335 0.473 6 0.970
85 Capparis pittieri 2.458 0.184 45 1.025
86 Casearea comersoniana 1.463 0.378 11 1.050
87 Guarea guidonia 0.996 0.262 24 1.074
88 Annona montana 0.840 0.525 6 1.077
89 Ocotea hartshorniana' 2.384 0.361 13 1.086
90 Perebea angustifolia 1.656 0.498 9 1.251
91 Eschweilera calyculata 1.685 0.473 10 1.252
92 Protium panamense 1.203 0.162 92 1.285
93 Ampelocera macrocarpa 1.047 0.562 8 1.332
94 Vitex cooperi 0.776 0.580 8 1.375
95 Protium costaricense 1.991 0.286 41 1.522
96 Lacmellea panamensis 0.748 0.577 10 1.529
97 Macrolobium costaricense 2.884 0.491 20 1.828
98 Licaria triandra 2.009 0.723 10 1.912
99 Swartzia simplex 5.483 0.883 7 1.951
100 Ocotea meziana 2.797 0.681 14 2.126*
101 Virola sebifera 1.393 0.351 74 2.502*
102 Quiina schipii 2.850 0.782 15 2.529*
103 Siparuna nicaraguensis 4.399 1.111 12 3.209**
104 Faramea terreyae 2.534 0.840 36 4.186***
' Canopy and subcanopy species with rapid growth rates and short lifespans (Lieberman et al. 1985a).
10 P<O.05 *,;.a
O .
G 00^
75 -4 - 0
?~50
z~~~~~~~~~~
< ~~EIULO CAOP COSR
0~~~~~~~~~~~~~~~~0
isinfcntl ligte codtin tha tre in geea (P d At .05).

-6 -4 -2 0 2 4 6
Figure 6. Residuals of canopy closure of individual trees belonging to the 104 most abundant species are
ranked according to Student's t (see text and Table 1). Each line of points represents a species; individual
trees are the points. The five species at the top of the figure have their crowns distributed in significantly
shadier conditions than trees in general (P < 0.05); the nine species at the bottom of the figure are distributed
in significantly lighter conditions than trees in general (P < 0.05).
largest individuals of this group may have their crowns in full sunlight. The
closure-size relationship appears quite similar among the four species groups.
For trees in each of the four growth behaviour groups, we compared the
residuals of the canopy closure index with the residuals of the population of
trees in general. Trees in Group 4 (fast-growing, short-lived species) were found
to occur in higher light environments than trees in general (t = 2.635, 3469 df;
P < 0.01). Trees in Groups 1, 2 and 3 did not differ significantly from trees in
general (P > 0.05). Thus understorey, subcanopy and long-lived canopy species
all occupy a random subset of available conditions in the stand (Figures 7a-c).
Although trees in Group 4 (species pooled) are distributed preferentially in
higher light levels, the nine species belonging to this group in fact live in a wide
(a) 20
os (a) Understorey spp.

x 15
z 0
LLJ.
10 %~~~~~~~~~~~~~~
10 0 .
* 00%
en * . C S
2 40 6 8 l
(b)
o 0~~~~~ ..:' **
20
((b)*2.
z~~~~~~~~~~~~~ S
o 10 o1000
..#/ DBH . *.#
(mm)
Li~~~~~~~~~~~~~S
1 0~~~~~~~~~~~~
0 0
(b) 20-0
> 15
0~~~~ ~ ~~~~~ IVA0.0
w~~~~~~~~~~
0 ~ ~ ~ ~~~~~~~~~~~~~0
canpysp cieDihln lfsas n (d) Su canpadsunopy sp ecepihrpi rwhrte n hr

o 0 0
lifespans.5
1 000 DBH (mm 00
Fiur 7 eltinsi btwe te anp cosr indexoV and tresz o re O mdhi aho h
Figurep7 Rpcelatih onshipfetweens thanopyd clnosur inde sbandotre speizes forh treesd gr10cmwdh inte eacdhofrth
lifespans.
(c) 20
oD (c) Long-lived canopy spp.

w i 15 x~~~~~~~~~~~~~~~~~~~~~~
Li
(d) 2 0 0~~~~~~~~~~~~
C) 10-
0~~~~~~~~~~~~~~~~ 0
((d*) 20s .*
1000 /DBH (mm)
CD(dd)stg20ig
O~~~ ~ ~ *..,,..:..;..* . .
>< 1 5 short-lived spp.
Li
0?
2 4 6 8 lo0
D 10
(n1) 0
o .
0 ~~~ 0 00
0 5~~~~~~~~~~~~
0 0 0 ~ ~ ~ ~ 0
0~~~~~~~~
2 4 6 8 10
1 000 /DBH (m m)
range of light environments (see Table 1 and Figure 7d). Group 4 species are
not ranked together in the highest light levels, and many of these species occupy
the available light conditions indiscriminately.
To determine whether species with lower shade tolerance occur within a
narrower range of light conditions than other species, we used an F-test to
compare the variance of the residuals of Group 4 (247 trees in 9 species) with
that of other trees (2184 trees in 37 species). The variances of the two groups
do not differ significantly (0.25 > P > 0.10). The breadth of the distribution is
not reduced in species occurring more commonly in higher light levels.
To test whether species differences in shade tolerance are more pronounced
among smaller size classes, we re-evaluated the data shown in Figure 6 but
included only individuals 20 cm dbh or smaller; such trees may be presumed
to be below canopy height (Lieberman & Lieberman 1994). The distribution
of residuals of small individuals does not differ in form from that of larger trees.
As before, the pattern is characterized by broad amplitude within species and
substantial overlap among species in the assemblages. Trees 10-20 cm dbh do
not show greater specificity in their use of the light environment than do larger
trees.
DISCUSSION
Our findings diverge from the predictions of classic gap-phase dynamics theory
in important ways. (1) Most of the 104 species studied are found over most of
the available range of light conditions, and 86.5% are distributed at random
with respect to present values of canopy closure. Thus virtually all species may
occur under both gap and non-gap conditions. (2) None of the species studied
is restricted to the high light levels associated with large gap conditions. Even
Hampea appendiculata and Cecropia obtusifolia, which had significantly lower mean
closure values than trees in general, occupy a large proportion of the range of
light conditions present. (3) Very high, uniform growth rates are associated
with open canopy conditions for some species but not others. Many of the
fastest-growing species in the stand (Hernandia didymanthera, Inga coruscans and
Stryphnodendron excelsum, for example) are distributed at random with respect to
canopy closure and are ranked near the middle of the list of species in Table
1. (4) Trees that belong to short-lived, fast-growing species were found as a
group to exhibit a significant preference for open conditions; yet they do not
occupy a narrower range of conditions than do other species, and thus are not
more specialized than other species. (5) Smaller individuals (10-20 cm dbh)
show the same pattern of breadth of distribution and overlap within the assem-
blage as is seen in larger individuals. Canopy conditions over the crowns of
young trees of fast-growing species are much the same as those of young trees
of other species. The idea of successional sequences or floristic cycles within
treefall gaps appears unfounded.
In evaluating the response of species to canopy closure, we have compared

species groups that are defined in terms of quantifiable life history character-
istics: size, maximum growth rate and projected lifespan. The categories thus
defined are independent of the variable of interest.
The results reported here pertain only to patterns of distribution. Further
analyses are needed to evaluate growth responses and reproduction of species
under varying light conditions.
Recent studies confirm that tropical tree species need not be highly special-
ized in their response to the light environment. Welden et al. (1991) found
89.6% of 106 sapling species on Barro Colorado Island to be 'generalists' in
their response to canopy conditions. Several recent studies have concluded that,
except for a small group of pioneer species (sensu Swaine & Whitmore 1988),
gap size has little or no effect on species composition (Kennedy & Swaine 1992,
Okali & Dike, in press, Raich & Gong 1990). Although fine-scaled differences
in species distribution have been reported within individual treefall gaps
(Brandani et al. 1988, Putz 1983, Uhl et al. 1988), the findings appear related
to soil disturbance, presence of woody litter and damage from falling debris,
and are not necessarily related to canopy closure.
The paradigm that tropical species in general occupy narrow, exclusive niches
was put forward in the 1960s as one (of many) explanations for the coexistence
of species in diverse assemblages. Subsequent authors have proposed that trop-
ical tree species conform to this trend, showing marked niche differentiation
from one another in their use of forest light environments (Denslow 1980, Orians
1982, Ricklefs 1977). An alternate view has more recently been suggested, in
which tropical forests are seen as assemblages of diffusely co-evolved, generalist
species (Hubbell & Foster 1986b). Critical evaluation of the two ideas has been
hindered by the lack of empirical evidence pertaining to whole assemblages.
The results presented here are in keeping with the latter notion, and lead us
to reject the view that tropical forests comprise tightly co-evolved, niche-
differentiated tree species. Instead of high specificity and narrow tolerance, we
find broad ecological amplitude; and rather than niche separation, we find a
pattern of extensive overlap among the great majority of species in the assem-
blage. There is no question that species are arrayed along a continuum of light
availability; but if we focus attention single-mindedly on each species' centre of
distribution rather than its range, we overlook the most noteworthy feature of
the pattern, namely the great congruence in species distributions in relation to
canopy closure.
We see from the foregoing that the tree species considered in this forest are
broadly capable of growing in the full range of conditions present - from open
areas, such as treefall gaps, to shaded areas, such as would be found under a
dense canopy. However, the vagaries of seed production and dispersal coupled
with the stochastic nature of forest dynamic processes may greatly reduce the
size of the species pool of available colonizers for any particular gap or establish-
ment site (Hartshorn 1980).
ACKNOWLEDGEMENTS
We are grateful to Victor Robles, who provided able field assistance. Roger
Anderson critically read the canopy closure algorithm. We thank M. D. Swaine
for useful discussions of the technique. Amos Bien, Rolf Borchert, D. M. New-
bery and D. P. Smith offered valuable comments on the manuscript. This work
was supported by National Science Foundation grants BSR-8117507, BSR-
8414968, EHR-9108770 and NASA grant NAGW-1033.
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Accepted 30 March 1994

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Canopy Closure and the Distribution of Tropical Forest Tree Species at La Selva, Costa Rica

Canopy closure and the distribution of tropical

MILTON LIEBERMAN,* DIANA LIEBERMAN,*

*Department of Biology, University of North Dakota, Grand Forks, ND 58202-9019,

mortality of individuals 310 cm dbh is from 2.03 to 2.34% y-', producing a

The index of canopy closure, G, is an estimate of shading at a given site based

Tree height was estimated allometrically using the empirical relation

Height = 5.5 dbh 3

1000 / DBH (mm)

CANOPY CLOSURE INDEX G

RESIDUAL OF CANOPY CLOSURE

RESIDUAL OF CANOPY CLOSURE

On the basis of growth rates, maximum diameters and projected lifespan,

1 Hampea appendiculata 1.188 -0.858 17 -2.960**

51 Pouteria neglecta 2.144 0.014 19 0.051

< ~~EIULO CAOP COSR

isinfcntl ligte codtin tha tre in geea (P d At .05).

RESIDUAL OF CANOPY CLOSURE

os (a) Understorey spp.

0~~~~ ~ ~~~~~ IVA0.0

canpysp cieDihln lfsas n (d) Su canpadsunopy sp ecepihrpi rwhrte n hr

1 000 DBH (mm 00

oD (c) Long-lived canopy spp.

1000 /DBH (mm)

>< 1 5 short-lived spp.

In evaluating the response of species to canopy closure, we have compared

Accepted 30 March 1994

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