Plant Ecol (2008) 196:233–244
DOI 10.1007/s11258-007-9347-0
Above- and below-ground competition between the liana
Acacia kamerunensis and tree seedlings in contrasting light
environments
Tarin Toledo-Aceves Æ Michael D. Swaine
Received: 27 June 2006 / Accepted: 10 August 2007 / Published online: 29 August 2007

Springer Science+Business Media B.V. 2007
Abstract Proliferation of lianas in canopy gaps can
restrict tree regeneration in tropical forests through
competition. Liana effects may differ between tree
species, depending on tree requirements for above-
and below-ground resources. We conducted an
experiment in a shade house over 12 months to test
the effect of light (7 and 27% external irradiance) on
the competitive interactions between seedlings of one
liana species and three tree species and the contribu-
tion of both above- and below-ground competition.
Seedlings of the liana Acacia kamerunensis were
grown with tree seedlings differing in shade toler-
ance: Nauclea diderrichii (Pioneer), Khaya
anthotheca (Non-Pioneer Light Demander) and
Garcinia afzelii (Non-Pioneer Shade Bearer). Trees
were grown in four competition treatments with the
liana: no competition, root competition, shoot com-
petition and root and shoot competition. Both root
and root–shoot competition significantly reduced
relative growth rates in all three tree species. After
one year, root–shoot competition reduced growth in
biomass to 58% of those (all species) grown in no
competition. The root competition treatment had a
T. Toledo-Aceves (&)
CONABIO, Insurgentes sur 4903, Col. Parques del
Pedregal, Mexico 14010 D.F., Mexico
e-mail: t.tarin@lycos.com; tarin.toledo@inecol.edu.mx
M. D. Swaine
School of Biological Sciences, University of Aberdeen,
Aberdeen AB24 3UU, UK
more important contribution in the effect of the liana
on tree growth. Tree seedlings did not respond to
competition with the liana by altering their patterns of
biomass allocation. Although irradiance had a great
effect on tree growth and allocation of biomass, the
interaction between competition treatments and irra-
diance was not significant. Nauclea diderrichii, the
tree species which responded most to the effects of
competition, showed signs of being pot-bound, the
stress of which may have augmented the competition
effects. The understanding of the interaction of
above- and below-ground competition between lianas
and trees and its moderation by the light environment
is important for a proper appreciation of the influence
of lianas on tropical forest regeneration.
Keywords Competition
Liana

Forest regeneration
Irradiance
Tree seedling
Introduction
Lianas (woody climbers) are an important component
of tropical forests, both floristically and in terms of
biomass (Gentry 1991). About 18–22% of the upright
plants in neotropical forest understories are juvenile
lianas (Putz 1984a). While liana biomass can be less
than 10% of total forest biomass they can contribute
up to 40% of the leaf biomass (Putz 1983). Their
abundance increases in forest canopy gaps and forest
edges where they represent important competitors for
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234
tree regeneration (Fox 1976; Putz 1984a; Fredericksen
and Mostacedo 2000; Schnitzer and Bongers 2002).
After lianas colonise gaps, the gaps can persist for
several years, arresting the forest succession (Putz
1984a; Schnitzer et al. 2000; Schnitzer and Carson
2001). They can affect tree regeneration by reducing
tree seedling survival and growth through mechanical
damage and resource competition (Dillenburg et al.
1993a; Dillenburg et al. 1995; Pérez-Salicrup 2001;
Schnitzer et al. 2005). Their negative effects on
regeneration in managed forests can be substantial as
lianas are more abundant in these systems (Campbell
and Newbery 1993; Schnitzer et al. 2000; Laurance
et al. 2001; Parren and Doumbia 2003).
The impact of lianas has been studied mainly
considering their above-ground effects (Putz 1984a;
Clark and Clark 1990; Schnitzer et al. 2000). How-
ever, recent studies have shown that lianas can also
have significant below-ground effects on tree perfor-
mance (Dillenburg et al. 1993b, 1995; Pérez-Salicrup
and Barker 2000; Grauel and Putz 2004; Schnitzer
et al. 2005). For example, below-ground competition
with lianas had more important effects on saplings of
the tree Liquidambar styraciflua than the above-
ground competition (Dillenburg et al. 1993b). Pérez-
Salicrup and Barker (2000) demonstrated that lianas
interfered with water availability for the tree Senna
multijuga in a dry tropical forest during the dry
season, with negative effects also recorded in tree
growth. However, lianas did not affect the leaf water
potential of the tree Swietenia macrophylla, showing
the diverse responses to lianas amongst tree species
(Barker and Pérez-Salicrup 2000). In a disturbed
tropical forest in Ivory Coast, Schnitzer et al. (2005)
found that while the competition with climbers for
above- and below-ground resources affected patterns
of biomass allocation in tree saplings, below-ground
competition alone had greater effects by reducing tree
sapling growth.
Lianas can have differential effects depending on
the tree species they colonise. Putz (1984b) and Clark
and Clark (1990) proposed that lianas affect saplings
of non-pioneer tree species more frequently than
pioneer species. In a light-rich environment, such as
gaps, the high growth rates of pioneers provide a
competitive advantage to escape quickly from the
liana competition. According to Schnitzer et al.
(2000) lianas might promote pioneer establishment
in gaps by prolonging the gap life and by reducing
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Plant Ecol (2008) 196:233–244
competition from shade tolerant species. Thus, the
effects of lianas on tree seedlings seem to be
affected by interaction with the light environment
and the tree light requirements. It is also likely that
tree seedlings will display a differential response to
above- and below-ground competition depending on
irradiance, but responses to this interaction have not
been investigated in detail. Different liana species
can also have different effects on their hosts
(Toledo-Aceves and Swaine 2007). In canopy gaps
the more light-demanding liana Acacia kamerunen-
sis significantly reduced the growth of tree
seedlings, while the more shade tolerant liana
Loeseneriella rowlandii had no effect on the trees
in a moist semi-deciduous forest (Toledo-Aceves
and Swaine in press).
The elucidation of the effects of light availability
on patterns of above- and below-ground competition
between lianas and tree seedlings is of great impor-
tance for tropical forest management. In this study,
we analysed the influence of high and low irradiance
on above- and below-ground competition effects
of the liana A. kamerunensis on three species of
tree seedlings of contrasting light requirements to
regenerate within a shade-house environment.
Methods
Tree species used were the pioneer Nauclea diderri-
chii (De Wild. and The. Dur.) Merrill (Rubiaceae),
the non-pioneer light-demander Khaya anthotheca
(Welw.) C.DC. (Meliaceae), and the non-pioneer
shade-bearer Garcinia afzelii Engl (Guttiferae) (eco-
logical guild sensu Hawthorne 1995; Table 1).
Within the non-pioneers, light-demanding species
are characterised by their higher requirements for
light and faster rates of growth and mortality, in
comparison with strongly shade tolerant species
(Hawthorne 1993). Nauclea diderrichii is a large
tree, typically present in high forest as scattered
individuals. It regenerates only in the presence of
sunlight; its small, photoblastic seeds (Kyereh et al.
1999) can remain dormant in the forest soil (Hall and
Swaine 1980) and are dispersed by elephants and
other animals (Hall and Swaine 1981; Hawthorne
1995). Khaya anthotheca, an African mahogany, is a
large evergreen or briefly deciduous tree with large
seeds dispersed by wind (Hall and Swaine 1981).
Plant Ecol (2008) 196:233–244
Table 1 Ecological guild, fresh seed mass, root:shoot ratio (mean ± 1 SE; N = 10) and dispersal syndrome of tree and liana species
(Hall and Swaine 1981, Swaine et al. 1997)
Species Guild Seed mass (g)
Nauclea diderrichii P 0.0003a
Khaya anthotheca NPLD 0.258 ± 0.01
Garcinia afzelii NPSH ca. 0.9
Acacia kamerunensis Liana 0.058 ± 0.003
P = Pioneer, NPLD = Non-Pioneer Light-Demander, NPSH = Non-Pioneer Shade-Bearer (Hawthorne 1995). Dry biomass based on
12–14-week old seedling measurements
a
Kyereh et al. (1999)
Garcinia afzelii is a small or medium-sized tree with
large seeds, common in dry forests and is widely used
in Ghana as chewing stick (Hall and Swaine 1981).
Acacia kamerunensis Gandoger (Mimosaceae) is a
large liana that reaches the upper canopy and is one
of the liana species most frequently recorded in
Ghana (Hall and Swaine 1981). It has bipinnate
leaves and thorns are present on the stem and rachis
enabling it to attach itself to other plants for support
during climbing. It is dispersed by wind and regen-
erates both in shade and in gaps but is more prolific in
gaps (pers. obs.). Its stems are used to make a coarse
sponge for teeth cleaning and other domestic uses
(Cunningham 2003). Species will be referred to by
their generic name.
The experiments were conducted in shade-houses
at the Forestry Research Institute of Ghana (FORIG),
Kumasi. The city of Kumasi is located in the forest
zone of Ghana (6430 N and 1380 W). The mean
annual precipitation for the area is about 1,500 mm,
with a mean annual temperature of 25.6C (Foggie
1947; Alder 1993). Kyereh et al. (1999) report a
relative humidity from 47% in January to above 85%
during the wet season. Plants were grown from seed
in April 2003 in a lightly shaded nursery at FORIG
and placed in the shade-houses four months later. The
treatments applied were: no competition (NC)—trees
were grown without liana; shoot competition (SC)—
tree and liana seedlings were grown in separate pots
but the liana was allowed to grow on the tree seedling
shoot; root competition (RC)—tree and liana seed-
lings were grown in the same pot and a bamboo stick
was provided as support to the liana, separating the
liana shoot from the tree seedling, to avoid above-
ground interference; root and shoot competition
(RSC)—tree and liana seedlings were grown in the
same pot allowing the liana to grow on the tree
235
Root:shoot ratio Dispersal syndrome
0.73 ± 0.24 Animals
0.69 ± 0.28 Wind
1.82 ± 0.47 Animals
0.77 ± 0.22 Wind
seedling, treatments following similar design in
Weiner (1986). The factorial design was 3 · 4 · 2,
where the factors and their levels were: three tree
species (Nauclea, Khaya and Garcinia), four compe-
tition treatments (NC, RC, SC, andRSC), and two
light conditions (7 and 27% PAR of full irradiance).
Four shade-houses were divided into two sections for
each light regime and there were six replicates per
treatment. In order to simulate daily variation in light
incidence and provide a neutral shade to plants,
wooden slats were placed in the roof and the sides of
the shade-houses. The spacing between sticks was
adjusted depending on the light regime required. In
this way the light alternates between high and low
irradiance and mimics more closely the forest sun-
fleck light environment (Whitmore 1996). Shade-
houses were covered by mosquito net to avoid
damage from insects, which did not alter the light
quality in terms of R:FR. The PAR in the shade-
houses was measured with a PAR sensor (Skye
Instruments, Data Hog) placed on the soil surface.
The required % irradiance was achieved when
measurements of at least three consecutive days had
approximately the same values. The sensors recorded
incident light at 1-min intervals in lmol m–2 s–1, over
24 h. PAR is reported as a percentage of full
irradiance recorded with another PAR sensor placed
in an adjacent open area.
Within the same shade-house, plants were reallo-
cated every month in a rotational pattern. To avoid
edge effects between light treatments 1 m of separa-
tion was left between the two light regimes. To
provide the plants with the same amount of soil per
individual, plastic pots of two dimensions were used:
pots of 28 cm diameter · 30 cm high were used for
NC and SC treatments and pots of 40 cm diame-
ter · 30 cm high for RC and RSC treatments. Pots
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were filled with forest topsoil and spaced 0.45 m
apart. The soil in all pots was maintained at field
capacity by daily watering.
Ten plants per species were harvested and oven
dried at 80C for 3 days to determine dry mass of
roots, stem and leaves at the beginning of the
experiment (August 2003, 4 months after germina-
tion). All plants were harvested for the final biomass
measurement after twelve months (September 2004)
and separated into roots, stems and leaves (including
petioles). Measurements recorded included: main
axis length, stem diameter at the base, number of
leaves and leaf area. Non-destructive growth mea-
surements were recorded after 6 and 12 months.
Leaf length and leaf maximum width were
recorded with a digital calliper, from a subsample
of 50 leaves per species, in order to estimate the leaf
area (LA). Photocopies were made of the leaves and
their leaf area was measured with a leaf area meter
(Delta T Image Analysis System). Based on these
values a regression equation was calculated for each
species. The regression coefficients were significant
for the four species (P \ 0.001; Nauclea r2 = 0.99,
Khaya r2 = 0.99, Garcinia r2 = 0.99, and Acacia
r2 = 0.92). The regression equation was used to
calculate the leaf area from subsequent measurements
of leaf length and maximum width.
The following growth parameters were derived
from basic measurements: relative growth rate in dry
biomass (RGRm = (lnW2–lnW1)/(T2–T1), where W2
and W1 are the final and the initial–total dry weight
per plant and T2–T1 is the time interval, month–1),
relative growth rate in height (RGRh, month–1),
relative growth rate in diameter (RGRd, month–1) and
relative growth rate in leaf area (RGRLA, month–1),
root mass ratio (RMR = roots dry weight/plant dry
weight), stem mass ratio (SMR = stem dry weight/
plant dry weight), leaf mass ratio (LMR = leaf dry
weight/plant dry weight), leaf area ratio (LAR = leaf
area per unit plant biomass, m2 kg–1) and specific leaf
area (SLA = leaf area per unit leaf dry weight,
m2 kg–1). The units used and calculations carried out
were taken from Hunt (1982), Lambers et al. (1998)
and Poorter (2001).
The effects and interactions of tree species, light
condition, and competition treatments, were analysed
with a GLM (Quinn and Keough 2002). Shade-
houses were considered as blocks. The data were
transformed using the Box-Cox transformation
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Plant Ecol (2008) 196:233–244
procedure before analyses, to increase homoscedas-
ticity. This transformation consists of the estimation
of a lambda (k) value to equalize the standard
deviation of a variable (Crawley 2002). The compar-
ison of means was done with the Bonferroni method
(Sokal and Rohlf 1995). All analyses were performed
in MINITAB Statistical Software (version 14.12).
Results
Growth and biomass allocation of trees under low
and high irradiance
Ambient (unshaded) irradiance averaged 23.33
(±0.88) moles m–2 day–1 when measured in April
2004. Daytime instantaneous irradiance exceeded
100 lmol m–2 s–1 for an average of 3 h in 7% irradiance
treatment and 7 h in 27% irradiance (with maximum
irradiance peaks of 358 and 663 lmol m–2 s–1, respec-
tively). For most tropical tree species 50 lmol m–2 is
above compensation point, including Pioneers (Riddoch
et al. 1991; Turnbull 1991; Kitajima 1994).
In response to these irradiances, tree species
growing without competition showed highly signif-
icant interspecific differences for all growth
parameters (Table 2) and all species showed signif-
icantly higher growth (especially in RGRm and
RGRd) in 27% than in 7% irradiance (Table 3).
The increase in RGRm in 27% over 7% irradiance for
the Pioneer, Nauclea (·3.9), was substantially higher
than for the Non-Pioneers, Khaya (·1.3) and Garcinia
(·2.2) (Table 3). After 12 months, Acacia attained
about twice as much total biomass as Nauclea, similar to
that in Khaya and about seven times more than
Garcinia; these differences were maintained in both
light regimes (Table 4).
The allocation of biomass was affected by irradi-
ance (Table 3), with greater allocation to roots in all
trees under high-irradiance, but differential responses
in SMR and LMR in each tree species (Table 3). The
Pioneer, Nauclea, assigned the highest proportion of
biomass to the roots, resulting in a reduced LMR and
under high irradiance LMR increased considerably at
the expense of a reduction in SMR. In contrast,
Khaya assigned a large proportion of its biomass to
the stem, independent of the light regime and
allocated less biomass to leaves under high irradi-
ance. Garcinia allometry had little to no response to
Plant Ecol (2008) 196:233–244 237

Table 2 Result of GLM analysis showing effects of tree seedlings of Nauclea, Khaya and Garcinia in competition with
species (S), light (L), competition (C), block and their the liana Acacia, after 12 months in shade-houses
interactions on growth parameters and biomass allocation for

RGRm RGRh RGRd RGRLA

df F P F P F P F P

S 2 64.46 *** 70.3 *** 26.72 *** 35.25 ***

L 1 22.95 *** 5.61 * 20.54 *** 8.82 **
C 3 5.92 *** 2.41 ns 5.83 *** 2.42 ns
S*L 2 2.78 ns 0.84 ns 1.11 ns 1.63 ns
S*C 6 0.65 ns 0.66 ns 0.23 ns 1.56 ns
L*C 3 1.13 ns 2.30 ns 1.92 ns 1.66 ns
S*L*C 6 0.45 ns 0.81 ns 0.74 ns 1.85 ns
Block 3 4.27 ** 7.52 *** 6.08 *** 4.71 **
RMR SMR LMR LAR SLA
df F P F P F P F P F P

S 2 21.41 *** 51.89 *** 86.94 *** 168.39 *** 627.29 ***
L 1 7.61 ** 5.46 * 0.01 ns 4.53 * 9.07 **
C 3 1.60 ns 1.39 ns 1.74 ns 4.13 ** 1.54 ns
S*L 2 2.77 ns 12.49 *** 13.59 *** 26.91 *** 1.27 ns
S*C 6 2.08 ns 2.86 * 0.33 ns 1.57 ns 1.28 ns
L*C 3 1.08 ns 0.52 ns 0.34 ns 2.64 ns 0.60 ns
S*L*C 6 2.86 * 1.29 ns 3.20 ** 3.22 ** 1.08 ns
Block 3 12.71 *** 2.86 * 6.78 *** 2.43 ns 2.08 ns
Degrees of freedom, variance ratios and level of significance (*P £ 0.05; **P £ 0.01; ***P £ 0.001; ns = non significant; n = 6)

the light treatment apart from the change in RMR.
The LAR in Nauclea increased considerably under
high irradiance while Khaya and Garcinia were not
significantly affected. Under high irradiance, there
was a significant reduction in SLA for all trees
(Table 3). The SLA decreased with species shade
tolerance (Nauclea [ Khaya [ Garcinia) while the
LMR followed the opposite pattern.
Competition effects of Acacia on tree seedling
growth and biomass allocation
The results from the GLM analyses showed that
competition with Acacia had significantly reduced
tree growth (Table 2), most clearly for RGRm and for
RGRd, but only with root and shoot (RSC) compe-
tition. RGRm under shoot competition did not differ
significantly from no competition in all three species
(Fig. 1) but caused a significant decline when in
combination with root competition. The effect was
similar in both 7 and 27% irradiances (no significant
interaction between competition and light treat-
ments). The negative effects of the competition
treatments increased in the sequence shoot \ root \
root and shoot (Table 3; Fig. 1). Overall results
show that root competition reduced tree growth by
23.7% while root and shoot competition reduced
growth by 42.2% in comparison to trees not exposed
to competition.
In general, the trees did not respond to the
competition with Acacia by altering their patterns
of biomass allocation, with the exception of LAR
(Table 2) and only in Nauclea in the low irradiance
treatment. There was some evidence for reductions in
LAR under shoot and under root competition, but no
difference from the control (no competition) for the
root–shoot competition treatment. In this treatment,
Acacia also showed higher LAR than in shoot or root
competition (data not shown) perhaps indicating a
more balanced competition between the climber and
its hosts in this latter treatment.

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Table 3 Relative growth rates, biomass allocation and leaf no competition (NC), root competition (RC), shoot competition
characters for seedlings of Nauclea, Khaya and Garcinia (SC) and root and shoot competition (RSC)
(mean ± 1 SE, n = 6) after 12 months in 7 and 27% PAR, in
Nauclea Khaya Garcinia
7% 27% 7% 27% 7% 27%

RGRd (cm cm–1 month–1)

NC 0.020 ± 0.01 a 0.063 ± 0.01 a 0.06 ± 0.01 a 0.12 ± 0.01 a 0.05 ± 0.01 a 0.10 ± 0.01 a
SC 0.029 ± 0.01 a 0.059 ± 0.01 a 0.11 ± 0.004 a 0.10 ± 0.01 a 0.05 ± 0.01 a 0.08 ± 0.02 a
RC 0.028 ± 0.01 a 0.034 ± 0.02 a 0.07 ± 0.01 a 0.11 ± 0.01 a 0.05 ± 0.01 a 0.08 ± 0.02 a
RSC –0.006 ± 0.03 b 0.029 ± 0.01 b 0.07 ± 0.01 b 0.07 ± 0.02 b 0.02 ± 0.01 b 0.06 ± 0.02 b
RGRLA (cm2 cm–2 month–1)
NC 0.29 ± 0.06 0.56 ± 0.05 0.56 ± 0.05 0.56 ± 0.01 0.36 ± 0.04 0.49 ± 0.02
SC 0.32 ± 0.03 0.53 ± 0.04 0.64 ± 0.01 0.63 ± 0.01 0.39 ± 0.05 0.37 ± 0.05
RC 0.44 ± 0.08 0.48 ± 0.05 0.55 ± 0.06 0.58 ± 0.06 0.38 ± 0.04 0.42 ± 0.03
RSC 0.38 ± 0.06 0.33 ± 0.08 0.55 ± 0.04 0.63 ± 0.07 0.30 ± 0.04 0.31 ± 0.02
–1
RMR (g g )
NC 0.58 ± 0.02 0.49 ± 0.03 0.24 ± 0.03 0.33 ± 0.02 0.31 ± 0.05 0.25 ± 0.02
SC 0.38 ± 0.02 0.44 ± 0.02 0.35 ± 0.02 0.36 ± 0.02 0.23 ± 0.03 0.34 ± 0.06
RC 0.41 ± 0.001 0.39 ± 0.06 0.27 ± 0.02 0.31 ± 0.01 0.31 ± 0.04 0.33 ± 0.03
RSC 0.32 ± 0.01 0.41 ± 0.01 0.27 ± 0.02 0.37 ± 0.04 0.33 ± 0.03 0.29 ± 0.03
–1
SMR (g g )
NC 0.50 ± 0.04 0.31 ± 0.01 0.30 ± 0.01 0.38 ± 0.02 0.22 ± 0.01 0.24 ± 0.01
SC 0.58 ± 0.02 0.35 ± 0.04 0.35 ± 0.02 0.35 ± 0.04 0.22 ± 0.01 0.27 ± 0.02
RC 0.32 ± 0.08 0.30 ± 0.07 0.39 ± 0.05 0.37 ± 0.05 0.24 ± 0.01 0.24 ± 0.02
RSC 0.52 ± 0.01 0.40 ± 0.03 0.29 ± 0.02 0.32 ± 0.08 0.22 ± 0.01 0.24 ± 0.02
–1
LMR (g g )
NC 0.09 ± 0.06 0.28 ± 0.03 0.45 ± 0.05 0.27 ± 0.01 0.46 ± 0.05 0.49 ± 0.03
SC 0.15 ± 0.008 0.23 ± 0.04 0.28 ± 0.02 0.28 ± 0.02 0.54 ± 0.04 0.37 ± 0.06
RC 0.07 ± 0.07 0.19 ± 0.04 0.32 ± 0.06 0.30 ± 0.05 0.44 ± 0.03 0.41 ± 0.02
RSC 0.02 ± 0.03 0.19 ± 0.03 0.43 ± 0.04 0.29 ± 0.06 0.44 ± 0.03 0.46 ± 0.03
LAR (cm2 g–1)
NC 42.92 ± 22.4 ab 62.43 ± 15.0 194.10 ± 32.3 80.34 ± 10.6 13.35 ± 2.99 16.63 ± 3.17
SC 15.67 ± 4.17 ab 85.88 ± 13.1 105.27 ± 5.61 82.02 ± 13.6 19.95 ± 5.44 10.10 ± 2.31
RC 4.96 ± 2.78 a 49.67 ± 9.89 128.00 ± 27.0 82.21 ± 12.9 11.66 ± 1.65 10.50 ± 1.18
RSC 61.05 ± 31.4 b 42.39 ± 8.22 163.23 ± 21.4 102.72 ± 33.2 12.63 ± 1.51 11.67 ± 0.57
SLA (m2 kg–1)
NC 63.63 ± 16.7 21.39 ± 37.3 41.94 ± 3.5 29.03 ± 3.7 28.08 ± 3.73 32.04 ± 4.49
SC 111.99 ± 66.1 40.95 ± 93.5 38.04 ± 4.2 28.62 ± 2.4 36.69 ± 10 26.90 ± 2.79
RC 46.33 ± 18.2 30.23 ± 57.9 40.19 ± 3.3 27.65 ± 2.6 26.34 ± 2.87 25.46 ± 3.53
RSC 33.61 ± 13.2 22.05 ± 20.3 38.21 ± 5.0 33.11 ± 3.9 28.68 ± 3.29 25.96 ± 2.25
Treatments differing at P \ 0.05 are represented with different letters; only comparisons between competition treatments within light
treatment are shown. Data were transformed for statistical analyses; non-transformed data are presented

Responses of Acacia to the competition with trees was significantly reduced when grown with Nauclea
compared with its growth with Khaya and Garcinia
The liana was affected differentially by the tree (Fig. 2), but because Acacia was not grown without
species with which it was competing. Acacia RGRm trees it was not possible to determine if Khaya and

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Plant Ecol (2008) 196:233–244 239

Table 4 Dry biomass (leaves, petioles, stem and roots) and height (mean ± 1 SE) of tree and liana seedlings before and after
12 months in shade-houses under 7 and 27% PAR
Biomass (g) Height (cm)
Initial Final Initial Final
7% 27% 7% 27%

Nauclea 6.95 ± 1.66 7.34 ± 1.80 16.58 ± 1.42 34.90 ± 3.85 41.00 ± 5.14 40.00 ± 3.84
Khaya 0.87 ± 0.12 16.27 ± 3.12 25.81 ± 3.31 12.27 ± 0.71 38.43 ± 3.89 44.87 ± 4.23
Garcinia 0.40 ± 0.12 1.83 ± 0.70 4.69 ± 0.69 6.65 ± 0.47 16.64 ± 2.29 21.83 ± 2.23
Acacia 0.96 ± 0.22 16.97 ± 1.06 25.39 ± 0.99 15.24 ± 2.00 146.5 ± 6.44 126.1 ± 6.10
All competition treatments are pooled for tree values, for Acacia, tree species and competition treatments are pooled

a 0.35 Competition
0.35 7% PAR
27% PAR c
a a ab b None c
0.30 0.30

Acacia RGRm (g g-1 mo-1)

Shoot bc
Root
0.25 ab
RGRm (g g-1 mo-1)

Root & Shoot 0.25 a a

0.20 a a ab b
0.20
0.15
0.15
0.10 a a ab b
0.10
0.05

0.00 0.05

-0.05 0.00
Nauclea Khaya Garcinia
b 0.35 a a ab b
Fig. 2 Differences in relative growth rate in dry biomass
0.30 a a ab b
(RGRm; mean + 1 SE) of the liana Acacia when grown with
the trees Nauclea, Khaya and Garcinia, under 7% (shaded) and
RGRm (g g-1 mo-1)

0.25
27% (unshaded) of PAR, after 12 months in shade-houses.
0.20 Competition treatments are pooled. Treatments not sharing
a a ab b
letters differed at P \ 0.05. Data were transformed for
0.15 statistical analyses; non-transformed data are presented

0.10
tendency for Acacia RGRm to be reduced in RSC
0.05 when planted with Nauclea but the effect was not
significant.
0.00
Nauclea Khaya Garcinia

Fig. 1 Effect of competition treatments, no competition, root Discussion

competition, shoot competition and root and shoot competition
on relative growth rate in dry biomass (RGRm; mean + 1 SE;
n = 6) of seedlings of Nauclea, Khaya and Garcinia under (a)
7% PAR and (b) 27% PAR, in shade-houses after 12 months.
Treatments not sharing letters differed at P \ 0.05, compar-
isons are between competition treatments within tree species
and light treatments pooled. Data were transformed for
statistical analyses; non-transformed data are presented
Garcinia affected its growth either negatively or
positively. Acacia had a greater RMR with Nauclea
than with Garcinia (Fig. 3) and had intermediate
values when planted with Khaya. There was also a
Several interacting factors may be expected to
influence plant responses to the competition. Avail-
ability of abiotic resources (light, nutrients and water)
will interact with plant size and age in ways which
differ amongst plant functional groups and species.
The precise pairing of climber and host species may
also lead to different outcomes. The age and size of
our experimental seedlings were similar (Table 4).
The liana species was selected as being potentially
aggressive and fast growing as indicated by a prior

123
240
0.6
a ab b also conformed to the expected effects of increases in
0.5
Acacia root mass ratio
0.4
0.3
0.2
0.1
0.0
Nauclea Khaya Garcinia
Fig. 3 Differences in root mass ratio (mean + 1 SE) of the
liana Acacia when grown with the trees Nauclea, Khaya and
Garcinia after 12 months in shade-houses. Competition and
light treatments are pooled. Treatments not sharing letters
differed at P \ 0.05. Data were transformed for statistical
analyses; non-transformed data are presented
experiment (Toledo-Aceves and Swaine in press) and
the tree species were chosen to represent a wide range
of shade tolerance. Our findings indicate that Acacia
competition for above- and below-ground resources
reduced the growth in biomass of all tree species, and
the effects were not modified by light availability.
Our results agree with other studies; liana impact on
tree growth was mainly through below-ground com-
petition. In our experiment, nutrient supply and water
availability were controlled as non-limiting, support-
ing the importance of below-ground competition.
Consequently, limitation of tree regeneration by
lianas in forest canopy gaps is likely to be due to
both above- and below-ground competition, because
of lianas’ superior capacity for acquiring water and
nutrients (Pérez-Salicrup and Barker 2000; Schnitzer
2005).
Acacia and tree seedlings responses to light
The longer but more slender stems of Acacia under
low irradiance compared with high irradiance prob-
ably reflect the strategy of plants in shade,
particularly for pioneer species, to invest in height
growth (Lambers et al. 1998; Poorter and Werger
1999). The responses of the tree species to the
light treatments without competition confirmed their
a priori classification into Pioneer, Non-Pioneer
Light-Demander and Non-Pioneer Shade-Bearer
123
Plant Ecol (2008) 196:233–244
(sensu Hawthorne 1995). Biomass allocation patterns
irradiance. RMR decreased in all species (Poorter
2001; Veneklaas and Poorter 1998) and SLA also
declined (Poorter 1999), except in the most shade-
tolerant species, Garcinia, in which there was little
change (Table 3). Low morphological plasticity in
biomass allocation patterns is characteristic of non-
pioneer species (Osunkoya and Ash 1991). However,
the lack of response in Garcinia to light could also
have been because the seedlings had not exhausted
their seed reserves by the end of the experiment.
Although its response to increased irradiance
conformed to the Pioneer model, Nauclea showed
poor growth compared with the other species (Fig. 1;
Table 4), even in the higher irradiance. In natural
conditions, Nauclea will outgrow Non-Pioneers in
moderate forest gaps (in the absence of shoot borers).
In this experiment, it seems probable that it became
pot-bound, as a result of its greater initial size
in comparison with the other species (Table 4).
McConnaughay and Bazzaz (1991) have shown that
restriction in root growth can limit biomass accumu-
lation independently of nutrient availability.
Competition for above- and below-ground
resources between trees and the liana Acacia
The results clearly show that Acacia competition
reduces tree growth and that below-ground compe-
tition has a greater effect than above-ground
competition. The importance of Acacia competition
for below-ground resources supports the findings of
previous studies (Weiner 1986; Dillenburg et al.
1993a, b; Pérez-Salicrup and Barker 2000; Schnitzer
et al. 2005) and our previous experiment conducted
in forest gaps (Toledo-Aceves and Swaine in press).
The effect of the root competition alone on tree
growth was statistically significant for Khaya after
6 months (data not shown), but disappeared after
one year. The effects of competition are expected
to increase with time, as a result of the increase in
competitor biomass and their consequent increase in
demand for resources. The reduction of the root
competition effects on Khaya indicate that the
competitive effects change during ontogeny. Dillen-
burg et al. (1995) found similar results for the tree
species Liquidambar styraciflua, which suffered a
Plant Ecol (2008) 196:233–244
reduction in the leaf photosynthetic capacity with
liana root competition, but the differences disap-
peared after two growing periods.
The lack of significant interaction between species
and competition treatment (Table 2) implies that the
responses of the three species to competition were
similar. Schnitzer et al. (2005) reported a similar
result: the reduction of tree sapling biomass caused
by lianas in the understorey of a disturbed forest in
Ivory Coast was irrespective of the species shade
tolerance. It is notable that Nauclea, already showing
poor growth in 7% irradiance, was precipitated into a
negative carbon balance when exposed to root and to
root–shoot competition (Fig. 1a).
According to the optimal partitioning theory
(Bloom et al. 1985), in response to the reduction
in the availability of below-ground resources, plants
would increase their investment in roots. However,
the effects of competition on biomass allocation to
roots reported in previous studies have found
contrasting results, which seemed to be greatly
influenced by the target species (Goldberg and
Fleetwood 1987; Casper et al. 1998; Osunkoya et al.
2005). Although Nauclea showed the highest RMR
of all species in all treatments, there were no
significant differences amongst the competition
treatments for any species for this variable (Table 3).
The converse response, less investment in leaves,
may also be expected and in our results this is shown
by LAR (but not in LMR) in Nauclea. For this
variable, the interactions between light and compe-
tition treatments and between species and
competition treatment were insignificant (as indeed
is the case for almost all measures) so that the
responses to competition did not differ amongst
species or irradiance.
Mutual negative effects between competitors
could explain the reduction in LAR in Nauclea with
root competition but not with root–shoot competition.
Acacia RGRm was reduced when grown with Nauc-
lea relative to its growth with Khaya and Garcinia.
Additionally, when grown with Nauclea, Acacia
allocated more biomass to the roots (Fig. 3) at the
expense of biomass allocated to the stem. In general,
liana roots have higher rates of extension than tree
roots so that they can colonize soil more rapidly (Putz
1991), which may explain the intense below-ground
competition and the limitation of soil volume
proposed here for Acacia.
241
It is notable that the tree species which shows most
responses to competition is the Pioneer, Nauclea,
which showed evidence of being pot-bound. This
stress is likely to have augmented the effects of the
treatments (negative RGRm and depressed LAR in
low light with RC and RSC). It is possible that the
effects of competition were not fully expressed with
the other species. Although the contribution of
below-ground competition to the interaction between
Acacia and tree seedlings explained most of the effect
on tree growth, an increase in the effects of above-
ground competition may be expected at a later stage.
Does the light environment moderate the
competition for above- and below-ground
resources between tree and Acacia seedlings?
Although irradiance clearly influenced tree growth
rates and biomass allocation, the effects of the
competition treatments were not altered by the light
regime. Below-ground competition seemed to play a
greater role in the effects of Acacia, but the absence
of a competition/light interaction was unexpected as
light can affect the response to below-ground
resources. For example, Osunkoya et al. (2005) found
that the increase in interspecific competition between
the tree Acacia mangium and Melastoma beccaria-
num, resulted in a higher allocation of biomass to
roots for the two competitors under 30% PAR (of full
sunlight) than under full sunlight. The intensity of
competition is expected to diminish with the increase
in the availability of resources (Wilson and Tilman
1993) so that stronger below-ground effects would be
expected in our 27% irradiance treatment, as a result
of the increase in competitor’s biomass. For example,
in a review of trenching experiments, Coomes and
Grubb (2000) showed that the effects of the removal
of below-ground competition have stronger effects on
seedling growth in gaps than in the forest understo-
rey, where availability of light is higher and therefore
the demand of nutrients and water is also higher.
In general, the intensity of competition depends on
both the resource availability and the competitor
biomass (Davis et al. 1998). It is possible that in 27%
irradiance the negative effects of the higher liana
biomass and the positive effects of the higher
irradiance on tree growth counteract each other so
that the net interaction effect was not different from
123
242
that under low light. Supporting this, the differences
in biomass among Acacia and the trees were similar
in both light treatments. Furthermore, the water
supply was the same in both light treatments, which
is different from natural forest conditions, where an
increase in irradiance may be accompanied by a
reduction in water availability. However, in forest
canopy gaps, reduction in competition intensity
related to improved availability of nutrients and
water has been reported (Veenendaal et al. 1996;
Denslow et al. 1998; Ostertag 1998; Lewis and
Tanner 2000).
The creation of gaps of particular dimensions has
been used in forestry in order to promote the
establishment of desirable timber species. Since large
gaps promote the establishment of pioneer trees and
also the proliferation of lianas, it is essential to
evaluate the effects of gap size on the interaction
between lianas and regenerating trees. Below-ground
competitive effects of lianas can have important
implications for forestry practices. As suggested by
Schnitzer et al. (2005), selective liana cutting beneath
the target tree crown can be an effective way to
minimize liana competition for both above- and
below-ground resources.
It is likely that the liana competitive effects would
increase in the forest, as a result of the different
conditions there. Although species probably root at
different depths in the forest, the environment in the
shade-house is characterised by more favourable
conditions than in the forest, with non-limiting water
supply and nutrient-rich topsoil, reducing the possible
competition for below-ground resources. Veenendaal
et al. (1996) reported that seasonal droughts in a
moist semi-deciduous tropical forest in Ghana aver-
age about 78 days per year. In seasonal tropical
forests, the main cause of tree seedling mortality is
water deficit (Lieberman and Mingguang 1992;
Gerhardt 1996), which is also the case in gaps
(Whitmore 1996). In seasonal tropical forests, the
superior ability of lianas to compete for below-
ground resources can be of great relevance for the
regeneration of trees (Schnitzer 2005).
In the forest, tree seedlings are frequently host to
more than one liana (Putz 1984a; Schnitzer et al.
2000), which would increase their impact as compet-
itive intensity increases with competitor biomass
(Keddy 1989). Deleterious effects, such as herbivory
and branch fall were also excluded in the shade-
123
Plant Ecol (2008) 196:233–244
houses. Slow growing species invest more resources
in defence than shade intolerant species (Coley et al.
1985). These attributes related to shade-tolerance
provide them with an advantage over pioneers in
the forest, but are irrelevant in a shade-house
environment.
In conclusion, Acacia competition for above- and
below-ground resources reduced the growth in bio-
mass of the trees, regardless of their shade tolerance.
Trees did not modify their allocation of biomass in
response to the competition with the Acacia. Differ-
ences in irradiance greatly affected plant growth and
biomass allocation but there was no evidence to
support differential effects of competition with
changes in irradiance. This study provides evidence
supporting a greater contribution of below-ground
competition in the interaction between liana and trees
at the seedling stage. Considering the dynamic nature
of the interaction between lianas and trees, the
evaluation of the effects at later stages of develop-
ment is needed to gain a fuller appreciation of the
impact of lianas on forest regeneration.
Acknowledgements This research was possible thanks to a
grant to T.T-A from Consejo Nacional de Ciencia y Tecnologı́a,
Mexico (ref. 128765). The Society for Experimental Biology
and the University of Aberdeen contributed with complementary
funds. We are grateful to M. A. Pinard and two anonymous
reviewers for the helpful comments on a previous version of the
manuscript. Assistance was provided by K. Macmillan for
the editing of the manuscript. The Forestry Research Institute
of Ghana provided all the facilities during the fieldwork. We
thank Paula Zamora and Peter Amoako for their assistance
in Ghana.
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