L ETTER
Lianas suppress tree regeneration and diversity in
treefall gaps
Stefan A. Schnitzer1,2* and
Walter P. Carson3
1Department of Biological
Sciences, University of
Wisconsin-Milwaukee, PO Box
413, Milwaukee, WI 53201, USA
2Smithsonian Tropical Research
Institute, Apartado 2072,
Balboa, Republic of Panama
3Department of Biological
Sciences, University of
Pittsburgh, Pittsburgh, PA 15260
USA
*Correspondence: E-mail:
Schnitzer@uwm.edu
Abstract
Treefall gaps are hypothesized to maintain diversity by creating resource-rich,
heterogeneous habitats necessary for species coexistence. This hypothesis, however, is
not supported empirically for shade-tolerant trees, the dominant plant group in tropical
forests. The failure of gaps to maintain shade-tolerant trees remains puzzling, and the
hypothesis implicated to date is dispersal limitation. In central Panama, we tested an
alternative biotic interference hypothesis: that competition between growth forms
(lianas vs. trees) constrains shade-tolerant tree recruitment, survival and diversity in gaps.
We experimentally removed lianas from eight gaps and monitored them for 8 years,
while also monitoring nine un-manipulated control gaps. Removing lianas increased tree
growth, recruitment and richness by 55, 46 and 65%, respectively. Lianas were
particularly harmful to shade-tolerant species, but not pioneers. Our findings
demonstrate that competition between plant growth forms constrains diversity in a
species-rich tropical forest. Because lianas are abundant in many tropical systems, our
findings may apply broadly.
Keywords
Barro Colorado Nature Monument, diversity maintenance, gap-phase regeneration,
lianas, Panama, treefall gaps, tropical forests.
Ecology Letters (2010)
I N TRODUCT ION
Periodic disturbances maintain plant species diversity in
many ecosystems. In tropical forests, treefall gaps are one of
the most common and important disturbances, and saplings
in the understory, which capitalize on light or other
resources in gaps, depend on gap formation to reach the
canopy. Gaps are hypothesized to maintain species diversity
via two key mechanisms. First, gaps extend forest resource
gradients by providing a high-light resource-rich regenera-
tion niche for some tree species, preventing their compet-
itive exclusion by more shade-tolerant species; evidence for
this mechanism is convincing, but only for pioneer tree
species (Brokaw 1985a, 1987; Brokaw & Busing 2000;
Schnitzer & Carson 2001; Schnitzer et al. 2008a). The
maintenance of pioneer tree species diversity, however,
provides only limited support for the gap hypothesis
because pioneers typically constitute only a small proportion
of the tree species and individuals in tropical forests (e.g.,
Dalling et al. 1998; Hubbell et al. 1999; Schnitzer & Carson
2001). Second, gaps may maintain diversity by providing a
heterogeneous and resource-rich environment in which
different tree species partition resources (e.g., Ricklefs 1977;
Denslow 1987). Within- or among-gap heterogeneity may
permit the coexistence of tree species that compete best at
some unique combination (or ratio) of resources within a
gap or among gaps of different sizes and ages (Brokaw 1987;
Brokaw & Busing 2000; Schnitzer et al. 2008a). Although,
gaps provide a more heterogeneous environment in tropical
forests than non-gap sites (Chazdon & Fetcher 1984;
Lieberman et al. 1995), there is little empirical evidence that
this heterogeneity is important to shade-tolerant trees
[reviewed by Brokaw & Busing (2000), Schnitzer et al.
(2008a)]. It remains puzzling why the diversity of shade-
tolerant trees, which comprise the vast majority of all tree
species, is not maintained by gaps when the critical limiting
resource (i.e., light) is suddenly and dramatically elevated.
One hypothesis for why gaps do not maintain the
diversity and abundance of shade-tolerant trees invokes
seed or dispersal limitation (Dalling et al. 1998; Hubbell
et al. 1999). This hypothesis posits that limited seed
production or seed dispersal, or both, prevent most tree
Ecology Letters, (2010) doi: 10.1111/j.1461-0248.2010.01480.x
 2010 Blackwell Publishing Ltd/CNRS
species from reaching treefall gaps in sufficient numbers for
resource partitioning to occur. An alternative and previ-
ously untested hypothesis is that interference and compe-
tition from non-tree plant growth forms, particularly lianas,
prevents recruitment or causes the displacement of tree
species that arrive in a gap. Lianas are abundant in most
tropical forests (Schnitzer & Bongers 2002; Schnitzer 2005),
where they compete intensely with trees indirectly through
resource competition, as well as directly through mechan-
ical stress (Putz 1984a; Pe?rez-Salicrup & Barker 2000;
Schnitzer et al. 2005; Toledo-Aceves & Swaine 2008). In
intact forest, lianas reduce tree growth and fecundity, and
increase tree mortality (Grauel & Putz 2004; Wright et al.
2005; Ingwell et al. in press). The effects of lianas may be
magnified in treefall gaps, where lianas are particularly
abundant and diverse (Putz 1984a; Schnitzer et al. 2000,
2008a, Schnitzer et al. 2004, Schnitzer & Carson 2001).
Nearly all studies on liana?tree interactions in gaps,
however, have been correlative or were not designed to
evaluate whether long-term competition from lianas is
severe enough to alter gap-phase regeneration and thereby
constrain the diversity and abundance of tree species within
gaps.
While lianas appear to harm most tree species in gaps,
they may actually facilitate the growth, recruitment and
survival of some tree species or guilds. Both Putz (1984a)
and Schnitzer et al. (2000) found a significant positive
correlation between liana abundance and pioneers species
abundance in gaps, whereas the correlation between lianas
and shade-tolerant trees was negative. These positive
correlations are unexpected given that lianas can smother
gaps, thereby arresting gap-phase regeneration (Schnitzer
et al. 2000). The answer may lie in the degree to which lianas
compete with pioneers vs. shade-tolerant species. For
example, Clark & Clark (1990) reported that < 1% of adult
pioneer trees at La Selva Biological Station in Costa Rica had
lianas in their crowns, whereas most of the shade-tolerant
trees hosted lianas. Pioneer trees may be buffered from the
deleterious effects of lianas because pioneers can avoid or
shed lianas through fast height growth, monopodial non-
branching stems, and large leaves that can dislodge attached
lianas (Putz 1984b). In contrast, shade-tolerant trees lack
these characteristics and are vulnerable to colonization by
lianas. Thus, lianas may facilitate pioneer tree regeneration
by reducing the recruitment and growth of competing
shade-tolerant trees (Schnitzer et al. 2000). To date, how-
ever, we lack long-term experimental tests of whether the
presence of lianas is unfavourable to shade-tolerant trees,
while at the same time favourable to pioneer species in gaps.
If the latter point is true, then gaps may enhance the
abundance and diversity of pioneer trees not only because
gaps are resource-rich habitats, but also because they are
habitats with relatively high liana abundance.
We conducted an 8-year liana-removal experiment on
Barro Colorado Nature Monument (BCNM), Panama, in
which we followed tree recruitment, growth and mortality in
gaps with and without lianas. We tested two main
hypotheses. First, lianas reduce overall tree growth, recruit-
ment, and survival in gaps, which results in lower tree
density and diversity (richness). If the presence of lianas
reduces tree growth, recruitment and survival in gaps, and
ultimately reduces diversity, then competition from lianas
may help explain why gaps fail to maintain tropical tree
species diversity because fewer tree species present limits
the potential for resource partitioning. Second, we tested the
hypothesis that lianas inhibit shade-tolerant tree growth,
recruitment, survival, and diversity in gaps, while facilitating
pioneer tree growth, recruitment, survival and diversity. If
lianas compete with shade-tolerant trees while concomi-
tantly facilitating pioneer trees, then we should find: (1)
lower shade-tolerant tree growth, recruitment, survival and
diversity in gaps with lianas than in gaps without lianas; and
(2) higher pioneer tree growth, recruitment, survival and
diversity in gaps with lianas than in gaps without lianas. To
our knowledge, this is one of the first in situ experimental
studies to evaluate whether competition constrains alpha
diversity in a tropical forest, and it may explain why gaps fail
to maintain shade-tolerant tree species diversity.
METHODS
Study site
We conducted the study on Gigante Peninsula, a protected
mainland forest that is located adjacent to Barro Colorado
Island and is part of the BCNM. Gigante Peninsula is
covered by a mix of early and late secondary seasonally
moist lowland tropical forest. Mean annual rainfall is
2600 mm, with a dry season from December until April
(Leigh 1999). For detailed information on the geology,
climate, flora and fauna of the BCNM, see Leigh (1999).
Gap selection, liana removal and vegetation census
In 1997, we located all (17) recent (< 1 year old) natural
treefall gaps on the fairly flat, upland central plateau of the
peninsula. Gap age was determined by the presence of the
fallen tree, and each gap was defined as the area, where a
vertical line from the edge of the canopy intersected the
ground (Van der Meer & Bongers 2001). Because gap edges
typically receive far more light and are more heterogeneous
than the intact forest (Van der Meer & Bongers 2001), we
extended our sampling 5 m into the gap edge zone. The
gaps varied in length, width, orientation and size; gaps were
145?499 m2, which comprises the most common gap sizes
in tropical forests (Brokaw 1985b; Sanford et al. 1986;
2 S. A. Schnitzer and W. P. Carson Letter
 2010 Blackwell Publishing Ltd/CNRS
Van der Meer & Bongers 2001). We paired gaps by size for
the purpose of randomly assigning treatments, either liana-
removal or un-manipulated control, and the liana-removal
and control gaps were statistically indistinguishable in total
gap area (ANOVA: F1,15 = 0.26, P = 0.62).
In each gap, we tagged, mapped, measured the diameter,
and identified to species all lianas and trees > 1.3 m tall. We
determined mean per-gap leaf area index (LAI) 1 month
before and 1 month after the liana removal in 13 randomly
selected gaps (five liana-removal and eight control gaps) by
measuring light 50 cm above the soil surface in three
locations in the southern half of each gap (facing directly
north) during the early morning and late afternoon using a
Li-Cor LAI-2000 leaf area index metre (Li-Cor Biosciences,
Lincoln, NE, USA). We recorded light simultaneously with a
second LAI-2000 located outside of the forest on the edge
of Lake Gatun to calculate relative LAI compared to open
sky. To ensure that our open sky measurements did not
intercept forest leaf area, we restricted light measurements
to the northern portion of the sky by capping the south-
facing half of the light sensors for both gap and open sky
measurements.
In the control gaps, where lianas were present, we scored
each tree in the census using the following scale: 0 = no
lianas in the tree crown, 1 = 1?25% tree crown covered,
2 = 26?50% tree crown covered, 3 = 51?75% tree crown
covered, 4 = 76?100% tree crown covered (follows Wright
et al. 2005; Ingwell et al. in press). In all gaps, we quantified
tree crown exposure to direct light for each tree using the
following scale: 1 = no direct light during the day,
2 = < 10% direct light during the day, 3 = 11?90% direct
light but with occasional crown shading during the day,
4 = direct exposure all day, but only the top or one side of
the crown (i.e., a canopy tree), 5 = direct exposure all day
for the entire crown (i.e., an emergent tree; method follows
Clark & Clark 1992).
We recensused the gaps again in 1998 to quantify tree
growth, recruitment, mortality, and the liana infestation and
canopy exposure indices, as well as to measure LAI. We
then cut all of the lianas in eight of the gaps, while nine gaps
remained as controls. We cut lianas near the forest floor
using machetes, but we did not attempt to remove the lianas
from the trees because of the risk of damaging the tree
crowns. In each gap, we cut an average of 109 (?17 SE)
lianas comprising 20 (?2 SE) species, and neither liana
abundance, diversity, nor basal area differed among removal
and control gaps prior to the cutting (F1,15 = 1.99,
P = 0.18, F1,15 = 0.56, P = 0.47, and F1,15 = 1.97,
P = 0.18, respectively). After the liana cutting, we visited
all gaps monthly for the first 2 months and bi-monthly for
the next 6 months to monitor the gaps and to cut
resprouting liana shoots in the removal gaps. Most liana
species resprout vigorously after cutting (e.g., Putz 1984a,
Schnitzer et al. 2004); however, after 8 months, the cut
lianas were no longer resprouting vigorously, and thus we
visited the gaps to monitor them and to cut resprouting
liana shoots every 3?4 months between censuses. All gaps
were revisited with the same approximate frequency and
intensity. We recensused the gaps in years 1999, 2000, 2001,
2003 and 2006 to quantify tree growth, recruitment,
mortality and the liana infestation and canopy exposure
indices. In early 2006, one of the liana-removal gaps was
completely covered by the crown of a newly fallen tree, so
we omitted this gap in 2006.
Data analysis
We analysed the effects of liana removal on mean per-gap
tree relative growth rate (RGR), tree recruitment, and
proportional tree mortality, using a repeated measures
random effects mixed model, where both treatment and
gap were factors (SAS Institute Inc., Belmont, CA, USA,
2007). RGR was calculated as: (ln(diameter1) ) ln(diame-
ter0)) ? (t1 ) t0), where diameter1 was the diameter (mm) of
an individual in a given census, diameter0 was the diameter
(mm) in the previous census, and t1 ) t0 was the difference
in years between sampling years. RGR was calculated in
mm year)1 for all individuals present in the study from 1998
to 2006 and we used mean RGR per gap for the analyses.
We calculated recruitment as the number of individuals per
gap that reached the 1.3 height limit and were not included
in the previous census. We calculated proportional mortality
for each census period as the number of individuals that
died between consecutive censuses divided by the total
number of individuals alive in the previous census period.
To determine whether lianas have a different effect on trees
with different life history strategies, we conducted these
same analyses on both pioneer and shade-tolerant tree
species separately, using the shade-tolerance classification
for trees on Barro Colorado Island (BCI) of Dalling et al.
(1998). We used t-test to compare the total species richness
of liana-free and control gaps after 8 years, as well as the
mean change in species richness per gap (final rich-
ness ) initial richness) over the 8-year period. We con-
ducted rarefaction simulations using Ecosim to test whether
differences in tree species richness between removal and
control gaps were due to differences in tree number (Gotelli
& Entsminger 2009). For each gap, we simulated the
number of tree species by randomly drawing 80 individuals
from the gap 1000 times. We then used a t-test to compare
the difference in density-independent species richness
estimates per treatment. We calculated the Bray?Curtis
index for presence ? absence and abundance and Jaccard
index for presence ? absence for all possible pair-wise gap
combinations and compared whether the tree community
differed in presence ? absence and abundance in the control
Letter Lianas suppress tree diversity 3
 2010 Blackwell Publishing Ltd/CNRS
and liana-free gaps using analysis of similarity (ANOSIM;
Clarke 1993), after removing singleton species. For all of the
above analyses, we transformed our data to normalize the
residuals when appropriate.
To test whether tree RGR over the 8-year period varied
with varying levels of liana infestation and exposure to light
in the control gaps (where lianas were present), we used an
ANCOVA with liana infestation and light scores as the factors
and stem diameter in 1998 as the covariate for all trees
combined, as well as for shade tolerant and pioneer trees
separately (SAS Institute Inc, 2007). Following the ANCOVA,
we used a Tukey HSD test to distinguish significant
differences among the liana and light scores. We used a
Wilcoxon Sign-Rank Test to determine whether removing
lianas significantly reduced gap-level LAI by testing whether
the difference in LAI immediately before and 1 month after
liana cutting deviated significantly from zero for the liana-
removal and control gaps (SAS Institute Inc, 2007).
RESUL T S
Growth, recruitment and mortality
Prior to the manipulation (1997?1998), tree recruitment,
growth (RGR), and mortality did not differ between the
controls and the gaps, where lianas were eventually removed
(P > 0.1 for all cases). Over the 8-year manipulation,
however, lianas significantly reduced tree growth and
recruitment in gaps. Mean tree RGR was higher in liana-
free gaps than in control gaps in all five censuses (Fig. 1;
repeated measures ANOVA: F1,15 = 4.90, P = 0.04), and was,
on average, 55% higher in the liana-free plots by the end of
the study period. Tree recruitment over the 8-year period
was also higher in liana-free gaps (F1,15 = 4.13, P = 0.06),
with a 46% higher cumulative increase in newly recruited
trees in liana-free gaps compared to control gaps (Fig. 2).
Tree mortality, however, did not differ significantly among
treatments (F1,15 = 0.93, P = 0.35; Fig. 2). Thus, the pre-
dominant effect of lianas on trees in gaps is the reduction of
growth and recruitment rather than survival. Nevertheless,
the total increase in trees (recruitment ) mortality) was 63%
higher in liana-free gaps than in control gaps.
Tree RGR in control gaps decreased sharply with
increasing canopy liana infestation (F4,694 = 5.69, P =
0.0002; Fig. 3a). This relationship was driven by the
significantly higher RGR in trees with no lianas compared
to trees with any level of liana infestation (Tukey HSD).
Tree growth did not increase with crown exposure to direct
light (Fig. 3b), although tree growth differed marginally
between canopy exposure levels 3 and level 4 (F4,693 = 2.07,
P = 0.08). Mean gap LAI decreased 1 month after cutting
lianas (TS = )6.5, P = 0.06, n = 5; Wilcoxon Sign-Rank
Test), but did not change in the control gaps (TS = )2.0,
P = 0.42, n = 8), demonstrating that lianas reduced light in
gaps (Fig. 4).
Species richness
Eight years after removing lianas, the increase in mean gap
tree species richness (final richness ) initial richness) was
65% greater in liana-free removal gaps than in control gaps
(t = 2.16, d.f. = 11, P = 0.026; Fig. 5). Prior to removing
lianas in 1998, tree species richness did not differ between
the liana-removal and control gaps (t = 0.719, d.f. = 15,
P = 0.24). After 8 years, tree species richness was margin-
ally higher in liana-free gaps than in the control gaps
(t = 1.44, d.f. = 14, P = 0.08). Rarefaction simulations
revealed that the higher species richness in liana-free gaps
was due to higher tree density, and richness did not differ in
liana-free and control gaps on a per-capita basis (t = 0.90,
d.f. = 11, P = 0.19). Tree community similarity did not
differ between liana-free and control gaps (Bray?Curtis:
R = 0.037, P = 0.25; Jaccard: R = 0.064, P = 0.21),
suggesting that the presence of lianas did not alter tree
community composition in gaps.
M
ea
n 
tr
ee
 R
G
R
 
1
0
0.1
0.2
0.3
2 3 5 8 
Years after liana cutting 
Figure 1 Mean tree relative growth rate (mm year)1) over the
8-year period (1998?2006) in gaps with lianas removed (dark bar
on left) and in control gaps with lianas present on Barro Colorado
Nature Monument, Panama. Error bars represent one standard
error.
M
ea
n 
pe
r 
ga
p 
tr
ee
re
cr
u
itm
en
t &
 m
or
ta
lit
y
1
0
25
50
75
100
125
2 3 5 8 
Years after liana cutting 
Figure 2 Cumulative recruitment (top two solid lines) from 1998
to 2006 of tree saplings on Barro Colorado Nature Monument,
Panama, into the 1.3 m tall size class in gaps with lianas (light lines)
and without lianas (dark lines). Bottom two dashed lines represent
cumulative tree mortality in gaps with and without lianas. Error
bars represent one standard error.
4 S. A. Schnitzer and W. P. Carson Letter
 2010 Blackwell Publishing Ltd/CNRS
Shade-tolerant vs. pioneer trees
The presence of lianas was particularly harmful to shade-
tolerant trees, which composed the vast majority of the trees
in this study. Mean shade-tolerant tree RGR was 56% higher
in the liana-free gaps than in the control gaps (F1,15 = 6.07,
P = 0.03). Likewise, mean RGR in the control plots was
significantly greater for shade-tolerant trees without liana
infestation compared to shade-tolerant trees with lianas in
their crowns (F4,619 = 5.49, P = 0.0002). In contrast,
pioneer tree RGR did not respond to liana removal
(F1,15 = 0.31, P = 0.59), and there was no significant
increase in pioneer tree growth with decreasing liana
infestation in the control gaps (F4,41 = 1.90, P = 0.13).
The increase in mean shade-tolerant tree species richness
from beginning to end of the study was 61% greater in liana-
removal gaps than in control gaps (13.0 vs. 8.0 species per
gap, respectively; t = 2.13, d.f. = 12, P = 0.027). The
increase in mean pioneer richness over the study period
was twice as high in removal gaps than in control gaps
(1.43 ? 0.37 vs. 0.67 ? 0.33; Wilcoxon v2 = 2.82, P = 0.09,
d.f. = 1), but the increase was an order of magnitude lower
than for shade-tolerant trees. Lianas did not significantly
affect recruitment or survival of shade-tolerant or pioneer
trees (P > 0.1 for all comparisons). Consequently, lianas
significantly reduced shade-tolerant tree growth and rich-
ness in gaps, slightly reduced pioneer tree richness, and had
no discernable effect on pioneer tree growth, recruitment or
survival.
D I SCUSS ION
Competition among contrasting plant growth forms
suppresses tree diversity
For more than three decades, gaps were thought to play a
major role in the maintenance of woody species diversity in
tropical forests (Ricklefs 1977; Brokaw 1985a,b; Denslow
M
ea
n 
tr
ee
 sp
ec
ie
s r
ic
hn
es
s
1998
30
35
40
45
50
55
60
2006 
Figure 5 Mean per gap tree species richness in 1998 and 2006 in
liana-removal and control gaps on Barro Colorado Nature
Monument, Panama. The mean per gap increase in tree species
richness was significantly greater in liana-removal gaps (14.4) than
in control gaps (8.7). Dark bars represent liana-removal gaps and
light bars represent control gaps. Error bars represent one standard
error.
Figure 3 Mean relative growth rates of trees in control gaps (where
lianas were present) with varying levels of crown liana infestation
(a) and canopy exposure to direct sunlight (b) on Barro Colorado
Nature Monument, Panama. Mean tree relative growth rate (RGR)
decreased significantly with increasing liana infestation. There was
no significant trend in tree RGR with increasing exposure to
sunlight, although tree growth differed significantly between tree
crown illumination index level 3 and level 4. Error bars represent
one standard error.
M
ea
n 
ga
p 
LA
I 
3
Liana removal Control
4
5
6
Figure 4 Mean leaf area index (LAI) in liana-removal and control
gaps on Barro Colorado Nature Monument, Panama. Dark bars
represent LAI before cutting lianas and light bars represent LAI
1 month after cutting lianas. Error bars represent one standard
error.
Letter Lianas suppress tree diversity 5
 2010 Blackwell Publishing Ltd/CNRS
1987). Canopy gaps elevate the key resource limiting growth
in the understory (light) and create a highly heterogeneous
habitat in the understory in terms of both resources and soil
disturbance. Thus, these habitats were thought to be engines
of plant recruitment and enhanced performance, particularly
for shade-tolerant tree species (Denslow 1995). While the
maintenance of diversity by gaps has been largely confirmed
for pioneer trees and lianas (e.g., Brokaw 1987; Schnitzer &
Carson 2001), it has been rejected for shade-tolerant tree
species (Hubbell et al. 1999; Brokaw & Busing 2000;
Schnitzer & Carson 2001). To date, the primary explanation
for why gaps fail to maintain shade-tolerant tree species
diversity is because seed and dispersal limitations prevent
tree species from arriving in gaps in sufficient quantity for
resource partitioning to occur (e.g., Hubbell et al. 1999;
Brokaw & Busing 2000). Our results provide an alternative,
though not mutually exclusive, explanation: gaps promote
the rapid recruitment and growth of lianas, which are
inimical to shade-tolerant tree species.
To our knowledge, this is one of the first studies to
demonstrate experimentally that interspecific competition
between contrasting growth forms can suppress species
richness in a tropical forest. Although correlative and short-
term experimental studies provide evidence that both palms
and lianas compete with trees (e.g., Putz 1984a; Farris-Lopez
et al. 2004; Grauel & Putz 2004; Schnitzer et al. 2000, 2005;
Wang & Augspurger 2006, Ingwell et al. in review), our
results demonstrate that these competitive effects are severe
enough to reduce shade-tolerant tree species diversity over
long time periods. Shade-tolerant tree species diversity
increased 61% faster in gaps without lianas than in control
gaps with lianas. Thus gaps, previously thought to benefit
shade-tolerant trees by providing elevated and heteroge-
neous resources, are also habitats that promote their
competitors. Indeed, lianas can become so abundant in
gaps that they can completely arrest gap-phase regeneration,
resulting in liana-dominated gaps that can remain at low
canopy height for decades (Schnitzer et al. 2000). The
relatively high increase in shade-tolerant tree species
diversity in liana-free gaps was driven by the increase in
density, which we confirmed with rarefaction analyses. By
suppressing shade-tolerant tree density in gaps, lianas also
suppress shade-tolerant tree diversity, thus limiting the
potential number of species that can partition resources.
Without sufficient numbers of species arriving and recruit-
ing into gaps, resource partition and niche differentiation
among species becomes unlikely, which is the fundamental
argument of the seed and dispersal limitation hypotheses, as
well as our biotic interference hypothesis. Thus, gaps likely
fail to maintain shade-tolerant tree diversity in tropical
forests because of a combination of biotic interference from
lianas, which constrains shade-tolerant tree recruitment and
diversity, as well as seed and dispersal limitations.
Lianas limit tree growth and recruitment in gaps,
particularly for shade-tolerant trees
Our experimental findings demonstrate unequivocally that
lianas reduce tree growth and recruitment in gaps,
presumably by a combination of above and belowground
competition, as well as through mechanical stress. Above
ground, lianas reduced light in gaps (Fig. 4), by increasing
the LAI (Kira & Ogawa 1971) and wood area index (WAI;
Sa?nchez-Azofeifa et al. 2009). Below ground, lianas appear
to be good competitors for water (Schnitzer 2005;
Schnitzer et al. 2005; Toledo-Aceves & Swaine 2008),
which may limit tree growth in gaps, particularly during
the dry season. Lianas cause mechanical stress by adding
considerable weight to the tree crown, thus forcing trees to
increase stem diameter at the expense of height (Schnitzer
et al. 2005; but see Toledo-Aceves & Swaine 2008). Our
findings indicate that lianas cause substantial decreases in
tree growth rates even when < 25% of the tree crown is
covered (Fig. 3). Our results are consistent with those of
Ingwell et al. (in press), who found that liana infestation of
trees in the BCI 50 ha plot significantly reduced tree
growth and, moreover, that trees with heavy liana
infestation were twice as likely to die than trees with few
or no lianas in their crowns.
Lianas may also reduce tree recruitment and thus diversity
in gaps by increasing the density of seed predators through
habitat-mediated indirect effects (sensu Royo & Carson
2008). Lianas provide pathways for mammalian seed
predators to traverse the forest canopy and to descend to
the forest floor (Emmons & Gentry 1983). Dense tangles of
lianas, which are common in tropical forests (Schnitzer et al.
2000), may provide privileged foraging sites for small
mammals by providing cover and protecting them from
predators (Emmons 1982). In many forests, small mammal
abundance is positively correlated with liana density (e.g.,
Lambert et al. 2006), and seed predation by mammals
increases with liana density (Kilgore et al. 2010). For
example, in central Panama, Kilgore et al. (2010) followed
the fate of palm seeds that were placed in the forest and
reported that seed removal and predation by mammals
increased strongly with increasing liana density. Conse-
quently, lianas not only compete with trees, but they may
provide pathways and protected foraging sites for small
mammals, which would further limit tree recruitment and
diversity in gaps.
Shade-tolerant trees, which comprise the majority of the
trees in tropical forests, have life history traits and
architectures that make them particularly vulnerable to
lianas (Putz 1984b; Schnitzer & Bongers 2002). These trees
tend to grow slowly and deploy many branches to maximize
light interception in the forest understory. In gaps, however,
these branches provide trellises that lianas use to climb and
6 S. A. Schnitzer and W. P. Carson Letter
 2010 Blackwell Publishing Ltd/CNRS
smother trees, which significantly reduces tree growth even
in the high resource gap environment (Schnitzer et al. 2000).
For pioneer tree species, we found no effect of lianas on
growth or recruitment. Schnitzer et al. (2000) proposed that
lianas give pioneer trees a growth advantage in gaps by
reducing the growth and abundance of competing shade-
tolerant trees. If so, then removing lianas should have
decreased pioneer performance. This prediction was not
supported by our data. Pioneer tree growth appeared to be
invariant to the presence of lianas in gaps, possibly because
of the high availability of resources and the ability of
pioneers to avoid liana infestation (Putz 1984b). Thus, the
positive correlation between lianas and pioneer trees in gaps
(Putz 1984a; Clark & Clark 1990; Schnitzer et al. 2000) may
be due to the ability of both groups to capitalize on high
resource availability rather than the indirect facilitation of
pioneers by lianas.
Distinguishing liana removal from biomass removal
While removing lianas resulted in significant increases in tree
growth, recruitment, and diversity in gaps, these types of
experiments suffer from the inability to disentangle the
effects of liana removal from plant biomass removal.
Nonetheless, four lines of evidence suggest that lianas have
a disproportionately strong competitive effect on tree
growth in relation to their biomass, and that removing an
equivalent amount of tree biomass (instead of liana biomass)
likely would not have produced the same results. First, lianas
have a far higher leaf mass and leaf area to stem diameter
(and biomass) ratio than trees, which may allow them to
photosynthesize and thus compete more per unit biomass
than trees. For example, Gerwing & Farias (2000) found
that lianas had 4?5 times greater leaf mass per stem diameter
than did trees. Second, lianas are able to reach the forest
canopy at very small stem diameters (2?3 cm; Kurzel et al.
2006), where they deploy their leaves and compete for light
and soil resources. Trees, in contrast, normally do not reach
the forest canopy until they are more than an order of
magnitude larger in diameter (Wright et al. 2005). Thus,
unlike saplings, lianas are likely to exert a strong competitive
effect even at small size classes. Third, we directly compared
the impact of cutting an equivalent biomass of lianas and
tree saplings on the performance of neighbouring trees
(M. Tobin, A. Wright, S. Mangan, & S. Schnitzer, unpub-
lished data). Neighbouring tree sap-flow velocity (a reliable
measure of plant performance) increased significantly
immediately after cutting lianas, but did not change after
cutting saplings, confirming that lianas can interfere with
tree water uptake and photosynthesis, whereas a similar
biomass of saplings did not. Fourth, if the growth response
from removing lianas in this study had been a biomass
effect, the effect should have been relatively short-lived.
Plant regeneration in treefall gaps is typically rapid, with gap
closure commonly occurring within 6 years of gap forma-
tion (e.g., Brokaw 1987; Fraver et al. 1998). If we had
witnessed a strict biomass removal effect, the liana biomass
that was removed should have been replaced by tree
biomass within a few years, and mean tree growth rates in
the liana-removal and control gaps should have become
equivalent. Instead, tree growth was lower in the control
gaps throughout the study, and the effect was particularly
strong 2 and 5 years after removing lianas (Fig. 1).
Increasing liana abundance: potential community and
ecosystem ramifications
Lianas may have strong community- and ecosystem-level
effects in forests, and recent studies have reported that
lianas may be increasing in abundance and biomass in
forests around the world (e.g., Phillips et al. 2002; Wright
et al. 2004; Chave et al. 2008; Ingwell et al. in press). Liana
abundance and biomass may be increasing due to elevated
CO2 or from changes in land-use, forest productivity or
rainfall (Phillips & Gentry 1994; Schnitzer 2005; Ko?rner
2006). While the actual causes of liana increases are not yet
known (Ko?rner 2006; Schnitzer et al. 2008b), the effects of
lianas on forest ecosystems may be substantial. As liana
abundance and biomass increase, tree growth, reproduction,
survival and diversity will likely decrease in both the intact
forest and in gaps (Wright et al. 2005; Ingwell et al. in press).
Increasing liana abundance and biomass may ultimately
reduce forest tree diversity and forest carbon sequestration
because lianas disproportionately displace trees with high
wood density (Schnitzer et al. 2000; van der Hejden &
Phillips 2009), and liana stems typically contain only a
fraction of the carbon in the trees that they displace
(Laurance et al. 1997; Schnitzer & Bongers 2002).
SUMMARY
Our findings demonstrate that competition from lianas
limits tree establishment, growth and diversity in gaps. While
previous studies focused on seed and dispersal limitation as
the explanation for why gaps may fail to maintain tree
species diversity in general, and shade-tolerant species
diversity in particular, our data show that biotic interference
and competition from lianas also reduces tree establishment,
growth and diversity. The effect of lianas on shade-tolerant
trees was particularly strong, whereas lianas appeared to
compete relatively little with pioneer trees. If lianas are
indeed increasing in abundance and biomass in tropical
forests, as reported in other studies, then shade-tolerant tree
recruitment, growth, and diversity in gaps will likely
decrease, while pioneer tree dynamics may remain largely
unaffected.
Letter Lianas suppress tree diversity 7
 2010 Blackwell Publishing Ltd/CNRS
ACKNOWLEDGEMENTS
We are grateful to S. Mangan, M.H.H. Stevens, and S.J.
Wright for advice on statistical analyses and for valuable
discussions. We thank N. Brokaw, E. Griffin, and two
anonymous referees for constructive comments on the
manuscript, L. Ingwell for help with data management, and
the undergraduate assistants who worked on this project.
Financial support was provided by NSF-DEB 0613666,
NSF-DEB 0845071, NSF-DEB 0212054, The Garden Club
of Allegheny County, and a Research Growth Initiative
award from the University of Wisconsin-Milwaukee. Logis-
tical support was provided by the Smithsonian Tropical
Research Institute.
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Editor, Marcel Rejmanek
Manuscript received 28 December 2009
First decision made 31 January 2010
Second decision made 17 March 2010
Manuscript accepted 21 March 2010
Letter Lianas suppress tree diversity 9
 2010 Blackwell Publishing Ltd/CNRS