BIOTROPICA 47(4): 449–458 2015 10.1111/btp.

12232

Elevation, Topography, and Edge Effects Drive Functional Composition of Woody Plant
Species in Tropical Montane Forests

Amira Apaza-Quevedo1,2,6, Denis Lippok1, Isabell Hensen1,3, Matthias Schleuning1,4, and Sabine Both5
1
Institute of Biology/Geobotany and Botanical Garden, Martin Luther University Halle-Wittenberg, Am Kirchtor 1, D-06108 Halle, Germany
2

s, Correo Central, Casilla, 10077 La Paz, Bolivia
Herbario Nacional de Bolivia, Universidad Mayor de San Andre
3
German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, D-04103 Leipzig, Germany
4
€r Naturforschung, Senckenberganlage 25, D-60325
Biodiversity and Climate Research Centre (BiK-F) and Senckenberg Gesellschaft fu
Frankfurt (Main), Germany
5
Institute of Biological and Environmental Sciences, University of Aberdeen, St Machar Drive 23, AB24 3UU Aberdeen, U.K.

ABSTRACT
Tropical montane forests comprise heterogeneous environments along natural gradients of topography and elevation. Human-induced
edge effects further increase the environmental heterogeneity in these forests. The simultaneous effects of natural and human-induced
gradients on the functional diversity of plant leaf traits are poorly understood. In a tropical montane forest in Bolivia, we studied envi-
ronmental gradients associated with elevation (from 1900 m to 2500 m asl), topography (ridge and gorge), and edge effects (forest edge
vs. forest interior), and their relationship with leaf traits and resource-use strategies. First, we investigated associations of environmental
conditions (soil properties and microclimate) with six leaf traits, measured on 119 woody plant species. Second, we evaluated changes in
functional composition with community-weighted means and functional structure with multidimensional functional diversity indices
(FRic, FEve and FDiv). We found significant associations between leaf traits and soil properties in accordance with the trade-off
between acquisition and conservation of resources. Functional composition of leaf traits shifted from the dominance of acquisitive spe-
cies in habitats at low altitudes, gorges, and forest interior to the dominance of conservative species in habitats at high altitudes, ridges,
and forest edges. Functional structure was only weakly associated with the environmental gradients. Natural and human-induced envi-
ronmental gradients, especially soil properties, are important for driving leaf traits and resource-use strategies of woody plants. Neverthe-
less, weak associations between functional structure and environmental gradients suggest a high redundancy of functional leaf traits in
this tropical montane forest.

Abstract in Spanish is available with online material.

Key words: acquisitive-conservative trade-off; Bolivia; fourth-corner analysis; fragmentation; functional diversity; functional structure; leaf traits.

UNDERSTANDING HOW ENVIRONMENTAL GRADIENTS
TIONAL DIVERSITY will be essential if we are to cope with human-
induced environmental changes (McGill et al. 2006). Functional
diversity (FD) refers to the value, range and relative abundance
of functional traits present in an ecosystem or a community. FD
is an important component of biodiversity and one of the major
determinants of ecosystem functioning (D
ıaz & Cabido 2001,
D
ıaz et al. 2007). Changes in components of FD have been
reported particularly along gradients of stress or disturbance and
have been associated with trait-based environmental filtering
along such gradients (Mouillot et al. 2013, Reich 2014). Despite
the increasing knowledge of the role of environmental gradients
driving plant traits in tropical lowland forests (May et al. 2013,
Fortunel et al. 2014), little is known regarding tropical montane
forests.
Received 26 August 2014; revision accepted 23 February 2015.
6
Corresponding author; e-mail: amiraelvia@yahoo.es
ª 2015 The Association for Tropical Biology and Conservation
DRIVE FUNC- Leaf traits are good indicators of FD across environmental
gradients because they reflect changes in plant resource-use strat-
egies. The strategies plants use to cope with the demands of their
environment are reflected in the energetic balance between invest-
ment in leaf production and photosynthetic returns (Reich 2014).
On the global scale, the widely accepted ‘leaf economic spectrum’
(LES) refers to an axis of plant strategies that range from species
with fast (acquisitive strategy) to slow (conservative strategy) pho-
tosynthetic return on investments of nutrients and dry mass in
leaves (Wright et al. 2004, Reich 2014). Acquisitive traits such as
high specific leaf area (SLA) and high leaf N concentration
(LNC) indicate rapid resource capture and high relative growth
rates, while the opposite applies for a conservative strategy
(Wright et al. 2004). Thus, although an acquisitive strategy pro-
vides advantages in high-resource environments, a conservative
strategy provides advantages when resources are low.
In tropical montane forests, soil fertility has been suggested
to be a key resource shaping species distribution and plant traits
449
450 Apaza-Quevedo, Lippok, Hensen, Schleuning, and Both
(Moser et al. 2007, Homeier et al. 2010). For example, leaf traits
corresponding to the LES are especially responsive to soil prop-
erties (Ordo~nez et al. 2009, Kr€ ober et al. 2012). Similarly, other
leaf traits such as stomata density (STD) and leaf carbon content
(LCC), which contribute to the regulation of plant resources
(Chapin et al. 1987, Sandquist & Cordell 2007), were shown to
be associated with soil nutrient levels (Kr€ ober et al. 2012). How-
ever, deficits of light and water can also reduce LNC and leaf
area (LA) so that less energy is required for the acquisition and
maintenance of N (Chapin et al. 1987). Thus, how the complex
interaction of several environmental gradients and their impact
on abiotic properties are reflected in community-level traits and
resource-use strategies remains unclear.
Elevation and topography are two major environmental gradi-
ents driving plant species composition in tropical montane forests
(Homeier et al. 2010). They may act simultaneously on the distribu-
tion of plant traits, mostly through indirect effects via soil properties
and microclimate. Elevation is one of the most important natural
factors driving leaf traits (Vel
azquez-Rosas et al. 2002, Read et al.
2013). Stress increases with elevation due to a decrease in tempera-
ture and soil nutrients (Soethe et al. 2008, Homeier et al. 2010, Lip-
pok et al. 2013). Thus, conservative plant strategies are favored at
higher elevations (Moser et al. 2007, Read et al. 2013). In addition,
local topography can drive leaf traits because of the abiotic heteroge-
neity created, e.g., ridges being more nutrient-poor, drier, and more
exposed to wind than slopes or gorges (Takyu et al. 2003, Lippok
et al. 2013). These conditions have been shown to increase leaf
thickness toward ridges (Takyu et al. 2003), which indicates a change
toward conservative plant strategies.
Now, habitat fragmentation constitutes an additional,
human-induced factor of environmental change in tropical mon-
tane forests (Killeen et al. 2005). Globally, only recently has more
emphasis been placed upon the effects of fragmentation on FD
(May et al. 2013, Magnago et al. 2014). One important conse-
quence of fragmentation is the formation of forest edges, whose
artificial and abrupt boundaries are associated with physical and
biotic alterations (Ewers et al. 2007). Forest edges can alter physi-
cal gradients, species distributions, and ecological processes (Lau-
rance et al. 2002). Edge effects lead to drastic changes in
environmental conditions such as lower moisture and higher tem-
peratures at forest edges compared to forest interior (Murcia
1995, Laurance et al. 2002). Effects on soil properties include
alterations of soil pH and soil moisture (Murcia 1995, Gieselman
et al. 2013) as well as increased soil C/N ratio at forest edges ver-
sus forest interior (Lippok et al. 2013). However, only a few stud-
ies have shown an effect of the abiotic changes associated with
edge effects on composition and variation in plant functional
traits (M€uller et al. 2007, Magnago et al. 2014).
Two important components of FD may change across environ-
mental gradients: the functional composition, which refers to the
presence and relative abundance of certain functional traits (D
ıaz &
Cabido 2001, Garnier et al. 2004), and the functional structure,
which describes the distribution of species and their abundances in a
functional space (Mouillot et al. 2013). The community-weighted
mean (CWM) has been proposed as a means to assess functional
composition, and to evaluate how mean trait values shift along envi-
ronmental gradients due to species selection (Garnier et al. 2004,
Lavorel et al. 2008). The CWM metric can reveal shifts in plant func-
tional trade-off strategy between rapid acquisition and conservation
of resources (D
ıaz et al. 2004, Wright et al. 2004). Environmental
changes can also alter the functional space of communities by
removing species or changing the abundance of species that are not
well adapted to the new environmental conditions (Mouillot et al.
2013). Multidimensional functional diversity indices like functional
richness (FRic), functional evenness (FEve), and functional diver-
gence (FDiv) shed light on the different aspects of functional diver-
sity and species assembly (Vill
eger et al. 2008, Mouchet et al. 2010,
Mouillot et al. 2013). These indices may decrease under extreme
environmental conditions; thus, they provide good indicators of the
effects of environmental change on functional structure (Mouillot
et al. 2013).
Here, we studied the complex interactions of components of
functional diversity and environmental gradients. We focus on FD
of leaf traits of woody plants in a tropical montane forest in the
Bolivian Andes, where we evaluated the effect of elevation (from
1900 m to 2500 m asl), topography (ridges and gorges), and edge
effects (edge forests and interior forest). We assumed that environ-
mental stress increased at higher altitudes, ridges, and forest edges
(Lippok et al. 2013) because harshness of microclimatic conditions
increases and nitrogen availability decreases along these gradients.
We expected to find: (1) associations between microclimatic and soil
variables and functional traits related to the trade-off in resource-use
strategies; (2) changes in functional composition along these envi-
ronmental gradients with a shift from dominance by species with
acquisitive traits at low altitudes, on gorges, and in the forest interior,
to dominance by species with conservative traits at higher altitudes,
on ridges, and at forest edges; and (3) changes in functional structure
with lower values of FRic, FEve, and FDiv at higher altitudes, on
ridges and at forest edges.
METHODS
STUDY AREA AND STUDY DESIGN.—We conducted the study near
Chulumani in the province of South Yungas, Bolivia. The area
corresponds to montane forests (Mueller et al. 2002). Mean
annual precipitation is 1459 mm, with the drier months occurring
between April and September (Molina 2005). The mean annual
temperature is 20.8°C. Fragmentation occurs prominently due to
anthropogenic activities in this region, which include agriculture
with crops of coffee, citrus fruits, and coca leaves (Killeen et al.
2005). As a result of the continuous impact of burning, huge
deforested areas, dominated by bracken and grass, have formed
along the slopes (Killeen et al. 2005). Due to this deforestation
following anthropogenic land use and disturbance, the remaining
forest vegetation remains mostly on the ridges and in gorges.
We investigated montane forest vegetation at six sites along an
elevation gradient of 600 m ranging from 1900 m to 2500 m asl
(appendix S1 in Lippok et al. 2013). To evaluate edge effects, we
studied forest edge (~ 20 m from margin) and forest interior
(>100 m from the edge), with two sampling plots (20 m 9 20 m)

per site (Fig. S1). We chose the plot size to sample structurally
homogeneous forest patches in this heterogeneous environment.
Bigger plots potentially include species shared among habitats,
hence reducing the representativeness of each habitat. To analyze
the impact of topography, we sampled one plot in the forest interior
on a ridge (and upper slope) and the other in a gorge (and lower
slope). Burning caused the loss of two plots; thus, for the analysis we
had to discard one plot at the forest edge and one on a ridge, leaving
22 plots.
ENVIRONMENTAL VARIABLES.—We measured the environmental
gradients of elevation, topography, and edge effects in a parallel
study performed on the same plots (Lippok et al. 2013). We
measured microclimatic variables related to temperature and
humidity in each plot with iButtons data loggers (Maxim/Dallas
Semiconductor Corp., Dallas, Texas, U.S.A.). Because we were
primarily interested in stress-related variables, we focused on
maximal temperature and minimal humidity. We installed data
loggers 20 cm above the ground in all plots within a site for at
least 1 month. We could not measure at all the sites simulta-
neously, so we measured each site in different months; the
sequence of measuring did not correlate with plot elevation. We
analyzed canopy openness based on nine hemispherical photo-
graphs taken at nine intercepts of a 10 m grid inside the plot
at 1.30 m above the ground, and analyzed digital images with
WinScanopy 2005.
We also determined soil properties within each plot. We
measured chemical soil properties from mineral soil samples cov-
ering an area of 100 m2, and took 12 sub-samples to a depth of
20 cm. We then air-dried and sieved (2 mm) the combined sub-
samples. Using the fine fraction (< 2 mm), we measured soil pH
potentiometrically in a 1:2.5 soil–H2O suspension. Contents of
exchangeable cations (Ca2+, Mg2+, and K+) were determined by
atomic-absorption spectrometry (AAS vario 6, Analytik Jena,
Germany), using 0.2 N BaCl2 as an extracting solution. We used
the sum of these three cations for further analysis. Soil carbon/
nitrogen ratio (Soil C/N) was determined on milled samples after
heat combustion (Vario ELIII elemental analyzer, Elementar, Ha-
nau, Germany).
LEAF TRAITS.—We obtained data on composition and abundance
of species in plots from another study (Lippok et al. 2013), which
considered all non-climbing woody plants (excluding ferns) with
diameter ≥2.5 cm at 1.3 m above the ground (diameter at breast
height, dbh). Individual rarefaction curves indicate that across all
plots, the previous study had sampled about 63 percent of plant
species (Fig. S2A). The ridges and in gorges, as well as in the
interior and forest edges, showed similar sampling intensities,
with comparable numbers of species sampled (Fig. S2 B, C, D).
We measured six leaf traits on 119 out of 259 species that
occurred across the 22 plots. Of the 119 species, 60 species
belonged to the most common species (84), whose cumulative
abundance made up at least 80 percent of the abundance across
all plots (Garnier et al. 2004). Considering the high number of
species, whose cumulative abundance made up the remaining 20
Functional Diversity in Tropical Montane Forest 451
percent, we included 59 out of the 175 less common species in
accordance with their likelihood of being collected. Overall, we
measured species traits representing 74 percent of the individuals
present (2178 individuals in total), and corresponding to about
67 percent of the total basal area (Fig. S3A and B). Across the
different treatments similar percentages of individuals were sam-
pled with regard to abundance as well as basal area (Fig. S3A
and B).
To reflect changes in the trade-off in resource-use strategies,
we evaluated SLA, LNC, LCC, and leaf C/N ratio, traits relevant
to the morphological and physical adaptations to soil fertility
(Chapin et al. 1987, Ordo~ nez et al. 2009). Microclimatic condi-
tions such as light and humidity can act as limiting resources and
regulate LA and stomatal conductance (Chapin et al. 1987). Thus,
we evaluated LA and STD as indicators of stomatal conductance
(Sandquist & Cordell 2007).
We measured at least three individuals per species for the
common species. However, given the low abundance of the less
common species, we could only sample one or two individuals
for around 50 percent of the species. Following Cornelissen et al.
(2003), we selected robust, well-grown plants located in a non-
shaded environment. Where possible, we sampled individuals of
the same species in different plots with leaves free from herbiv-
ory. We collected at least ten leaves per individual and stored
them in plastic bags for transportation.
In the field laboratory, we gently blotted five leaves with tis-
sue paper to remove any surface water or dust, and scanned the
leaf without the petiole. We stored the leaves in paper bags and
dried them in the oven at 60°C for at least 72 h before measur-
ing their dry masses. We processed the scanner images with the
Win FOLIA Pro S program (Regent Instruments Inc.) to obtain
the LA and calculate SLA. We dried the remaining leaves at 60°C
for 72 h and measured total N and C per unit of dry leaf mass
with the CN Vario ELIII elemental analyzer (Elementar, Hanau,
Germany), to calculate LNC, LCC, and the C/N ratio.
We measured STD—defined as the number of stomata per
unit area of leaf surface—from leaves stored in 70 percent etha-
nol. We cut the upper surface of leaves with a razor blade (Spi-
cher 1985) on an area free of venation in or near the middle of
the leaf. We obtained images of stomata with a light-optical
microscope (Zeiss Axioskop 2 plus) and analyzed them using
Axio Vision Software (v. 3.0).
STATISTICAL ANALYSIS.—To evaluate the association between leaf
traits and microclimatic and soil variables, we applied a fourth-
corner analysis (Legendre et al. 1997). This method allows testing
of statistical associations between functional traits and continuous
environmental variables, related by species abundances under the
respective environmental conditions (Dray & Legendre 2008).
Thus, the fourth-corner analysis tests if the environmental gradi-
ents studied cause continuous and direct changes in specific leaf
traits.
A principal component analysis showed that soil C/N ratio
was independent from the other environmental gradients, while
maximum temperature and canopy openness were positively cor-
452 Apaza-Quevedo, Lippok, Hensen, Schleuning, and Both

related, and both variables were negatively correlated with mini- FUNCTIONAL TRAITS AND ENVIRONMENTAL VARIABLES.—The fourth-
mum humidity (Fig. S4). In addition, soil pH and cations were corner analysis revealed significant associations between leaf traits
positively correlated. Therefore, to avoid collinearity between and soil properties, mainly for SLA, LNC, and C/N (Table 1).
environmental predictors, we applied the fourth-corner analysis SLA and LNC were negatively related to soil C/N and positively
considering only three representative environmental variables (soil related to pH. LA was also negatively associated with soil C/N,
C/N ratio, soil pH and maximum temperature). For significance but unrelated to pH. Leaf C/N was positively associated with soil
testing, we ran 999 permutations and used a combination of per- C/N and negatively with pH. Neither LCC nor STD was affected
mutation methods 2 (entire sites permuted) and 4 (entire species by any environmental variable. Microclimate did not show associ-
permuted; Dray & Legendre 2008) and took the larger of the ations with leaf traits.
two P-values, as suggested by Ter Braak et al. (2012). To account
for differences in total abundances among plants, we Hellinger- FUNCTIONAL COMPOSITION.—Overall, mean values (SD) of the
transformed the relative abundances of species prior to the analy- CWM for each trait in the 22 plots were: SLA = 12.10 mm2/mg
sis (Legendre & Gallagher 2001). ( 2.28), LA 9062.03 mm2 ( 1938.16), LNC 1.89% ( 0.3),
We measured functional composition by community- LCC 44.92% ( 1.27), STD 288.41 1/mm2 ( 48.11), and C/
weighted means (CWM), defined as the mean trait values pres- N = 26.19 ( 4.23). Functional composition showed a shift from
ent in the community, and weighted by the relative abundance an acquisitive strategy, reflected by higher CWM of SLA and
of the species in the community (Lavorel et al. 2008). We evalu- LNC at lower altitudes, in gorges and forest interiors, to a con-
ated functional structure by multidimensional functional diversity servative strategy with low trait values at high altitudes, on slopes
indices (Vill
eger et al. 2008). Multidimensional measures of these and at edges (Fig. 1A and B). By contrast, the CWM of C/N
traits are based on the convex hull hyper-volume (Cornwell ratio showed an opposite shift with significantly increased values
et al. 2006), where species are arranged according to their traits at higher elevations, on slopes and at edges (Fig. 1C). Similar to
in a multidimensional functional space (Vill
eger et al. 2008). SLA, LA tended to decrease with elevation and was lower at the
Thus, FRic refers to the value of the convex hull volume filled forest edge than the forest interior, but no significant difference
by a community. FEve quantifies the regularity with which the was found in relation to topography (Fig. 1D). STD and LCC
functional space is filled by species, weighted by species’ abun- were not responsive to any factor evaluated (Fig. 1E and F).
dance, and FDiv refers to the proportion of abundance sup-
ported by species having the extreme trait values within a FUNCTIONAL STRUCTURE.—When we compared the multidimen-
community (Mouillot et al. 2013). We calculated indices for each sional functional diversity indices of leaf traits along the environ-
plot. Following the suggestion of Vill
eger et al. (2008), we calcu- mental gradients, FRic showed significant differences with respect
lated FRic, FEve, and FDiv without considering leaf C/N ratio
as it derives from other traits (LNC and LCC). With the met-
rics of functional composition and structure, we performed lin- TABLE 1. Fourth-corner analysis of leaf traits and environmental variables of woody
ear mixed effect models with elevation, topography, and edge species in a tropical montane forest. The analysis is based on a combination
effects as the fixed factors and site as a random factor. We of permutation methods 2 and 4. Significant P-values (P < 0.05) are
standardized trait values to zero mean and unit variance for the printed in bold and based on 999 randomizations. Correlation coefficient (r)
fourth-corner analysis and for the functional indices. Prior to and their direction () are given for each correlation. Soil (C/N) = soil
standardization, we log-transformed all traits, except STD, which C/N ratio, pH = soil pH, Max. temp = maximum temperature (˚C),
we square-root transformed. All analyses used R 2.15.2 (R Core LA = leaf area (mm2), SLA = specific leaf area (mm2/mg), LNC =
Team 2012; R Foundation for Statistial Computing, Vienna, leaf nitrogen content (%), LCC = leaf carbon content (%), STD =
AT). We used the R-packages ‘vegan’, ‘nlme’, ‘ade4’, and FD stomatal density (1/mm2), C/N = leaf C/N ratio.
(Lalibert
e & Shipley 2011).
Leaf Trait Soil (C/N) pH Max. temp.
RESULTS LA r-value 0.192 0.063 0.06
P-value 0.009 0.348 0.361
ENVIRONMENTAL VARIABLES.—Soil C/N ratios were higher at for- SLA r-value 0.304 +0.272 0.15
est edges and ridges (Fig. S5A), while exchangeable cations and P-value 0.001 0.001 0.079
soil pH were lower in ridges than in gorges (Fig. S5B and C). LNC r-value 0.321 +0.242 0.16
Maximum temperature was higher at forest edges (mean of P-value 0.001 0.008 0.086
26°C) than in the forest interior (mean of 23°C; Fig. S5D). Mini- LCC r-value +0.068 0.075 0.01
mum humidity of edges (mean 65%) and ridges (mean 70%) was P-value 0.352 0.232 0.821
lower than in the forest interior (mean 79%) and gorges (86%; STD r-value 0.006 0.0003 0.03
Fig. S5E). Canopy openness did not change across any gradient P-value 0.901 0.975 0.528
(Fig. S5F). Further details about changes in microclimate and soil C/N r-value +0.306 0.236 +0.12
properties across the environmental gradients can be found in P-value 0.001 0.008 0.146
Lippok et al. (2013).
 Functional Diversity in Tropical Montane Forest 453

FIGURE 1. Variation in CWM of leaf functional traits along elevation, topography, and edge effects in a montane forest of Bolivia. (A) SLA (specific leaf area; mm2/
mg), (B) LNC (leaf nitrogen content; %), (C) C/N (carbon/nitrogen ratio), (D) LA (leaf area; mm2), (E) LCC (leaf carbon content; %), (F) STD (stomatal density; 1/
mm2). Number of plots per factor: Elevation (22), Edge effects (11 at the edge and 11 in interior), and Topography (6 in gorges and 5 in ridges). Analysis based in 119
woody species. The figure shows untransformed values; however, P-values and the respective linear mixed effect models are based on transformed trait values.
454 Apaza-Quevedo, Lippok, Hensen, Schleuning, and Both
to topography, with higher values on ridges than gorges, but no
differences with respect to elevation or edge effects (Fig. 2A).
FEve and FDiv were not significantly affected by any of the envi-
ronmental gradients studied (Fig. 2B and C).
DISCUSSION
In Bolivian montane forests, environmental gradients related to
elevation, topography, and forest edges affected the distribution
of leaf traits in woody plant communities. We found: (1) leaf
traits had a direct relationship with soil properties, but not with
microclimate; (2) leaf trait-environment relations were associated
with changes in functional composition, describing a gradient
from acquisitive to conservative strategies with respect to eleva-
tion, topography, and edge effects; and (3) changes in functional
structure were generally weak and only evident for FRic in rela-
tion to topography.
DIRECT RELATIONSHIPS BETWEEN LEAF TRAITS AND ENVIRONMENTAL
VARIABLES.—We demonstrated that leaf area (LA), specific leaf
area (SLA), leaf nitrogen content (LNC), and leaf carbon/nitro-
gen (leaf C/N) were responsive to soil properties. These associa-
tions support the hypothesis that leaf traits reflecting resource
acquisition are more prominent in nutrient-rich soils (Coomes
et al. 2009, R
ejou-M
echain et al. 2014). Given that low values of
soil C/N ratios indicate high nutrient availability (Ordo~nez et al.
2009), its negative relationship with LA, SLA, and LNC and a
positive association with leaf C/N suggest a resource conserva-
FIGURE 2. Variation in multidimensional functional diversity indices along elevation, topography, and edge effects in montane forests of Bolivia. (A) FRic =
functional richness. (B) FEve = functional evenness. (C) FDiv = functional divergence. P-values and the respective test statistics were derived from linear mixed
effect models. Number of plots per factor: elevation (22), forest edge/interior (11 each), and topography (6 in gorges and 5 in ridges). The analysis is based on
119 woody plant species.
tion strategy in less-fertile soils. Consistent with Kr€ ober et al.
(2012), we also found positive associations between soil pH with
SLA and LNC and a negative association with leaf C/N, which
indicate resource conservation under acid soil conditions. Soil
acidity was reported to be closely related to lower soil fertility
and, thus, facilitate a conservative plant strategy (Schaik & van
Mirmanto 1985).
Neither leaf carbon content (LCC) nor stomata density
(STD) were responsive to any environmental variable. Unexpect-
edly, our study did not support significant associations of LCC
and environmental gradients. LCC reflects investment of
resources into structural tissues (Albert et al. 2010) and may
increase as part of a conservation strategy (Pakeman et al. 2009).
In addition, immobile defences such as tannins or lignins can be
part of a conservative strategy (Coley 1988). As we did not mea-
sure secondary compounds, we cannot rule out the possibility
that simultaneous changes in LCC and defence components
could obscure direct associations of LCC with environmental fac-
tors. Similarly, decreases of humidity at forest edges and ridges
compared to forest interior and in gorges were not reflected in
overall community-level characteristics. Other studies reported
that STD is significantly affected by air humidity, water availability
(Woodward & Kelly 1995), and exposure to high light levels
(Givnish 1988). However, STD did not show any significant
change across the studied environmental gradients. As STD vari-
ability in species is high in species-rich tropical forest (Camargo
& Marenco 2011), a direct response of STD to environmental
variables might be masked on the community level. Other physi-

ological mechanisms such as a reduction in LA that balance the
trade-off between carbon gain and water loss (Chapin et al. 2002)
may additionally reduce the effects of environment on STD.
The lack of associations between leaf traits and microclimatic
variables is unexpected and requires an explanation. The objec-
tives of this study led to the establishment of relatively small
sampling plots of 20 m 9 20 m. We chose the size to keep the
environmental conditions and species composition homogeneous
along the gradients studied. These plots were not fully representa-
tive, capturing around 63 percent of the species composition of
the forests. However, similar representativeness covered among
habitats indicates that the plot size was adequate for comparing
gradients.
FUNCTIONAL COMPOSITION.—As predicted, shifts of community-
weighted means (CWM) across environmental gradients reflected
the plant trade-off strategy of resource use (D
ıaz et al. 2004).
Supporting previous studies (Moser et al. 2007, Soethe et al.
2008, Read et al. 2013), CWM of SLA and LNC significantly
declined with elevation, and LA showed a decreasing trend. Thus,
plant communities studied in our Bolivian montane forest were
similarly less productive at high altitudes than at lower altitudes
(Raich et al. 1997, Kitayama & Aiba 2002), with low nutrient
acquisition and nutrient deficiency (Soethe et al. 2008). An
increase in CWM of leaf C/N reflects leaf structure investment
in these less productive environments (Poorter & de Jong 1999),
and supports the notion that species with conservative strategies
increase in dominance with higher elevation (Vel
azquez-Rosas
et al. 2002, Moser et al. 2007, Read et al. 2013). In addition,
ridges are drier habitats with less-fertile soils than that found in
gorges (Lippok et al. 2013), and therefore presumably offer more
stressful habitats. Indeed, we found low values of CWM of SLA
and LNC, and high values for C/N at ridges, consistent with our
hypothesis and previous literature (Takyu et al. 2003). As pointed
out by Homeier et al. (2010), elevation and topography can lead
to small-scale mosaics of edaphically different habitats, which
promote high species richness of trees in tropical montane for-
ests. Our results indicate that through trait filtering, elevation and
topography also promote heterogeneous community traits values.
This is also supported by the high species turnover observed in
these forests (Lippok et al. 2013).
In the tropical montane forest in Bolivia, edge effects lead
to environments with less-fertile soils and with harsh microcli-
matic conditions (Lippok et al. 2013). Our data reveal that habi-
tats at forest edges are more stressful than the forest interior, due
to increased temperature, lower air humidity, and lower soil fertil-
ity. Edges, therefore, favor species with a conservative strategy.
Hence, edge effects can translate into shifts of plant strategies
and highlight the relevance of fragmentation in filtering traits and
driving species distributions (M€uller et al. 2007, Magnago et al.
2014). Given that changes in functional composition are associ-
ated with changes in ecosystem processes (Hooper et al. 2005,
Reich 2014), this suggests that ecosystem productivity might
decrease along forest edges, due to a dominance of species with
conservative leaf traits (Chapin 2003). Other consequences of
Functional Diversity in Tropical Montane Forest 455
such changes in CWM of leaf traits can be reflected in decreased
decomposition rates causing altered nutrient cycling at forest
edges (Cornwell et al. 2008, Bakker et al. 2011).
FUNCTIONAL STRUCTURE.—We did not find significant differences
in FRic, FEve, or FDiv across any environmental gradient, except
for changes in FRic with regard to topography. Consistent with
de Bello et al. (2012), we found higher values of FRic at ridges
than at gorges. Pakeman (2011) reported high values of FRic at
intermediate levels of productivity and disturbance. This could
suggest that the ridges we studied in the Bolivian montane forest
represent intermediate environmental conditions, rather than
environmental extremes, promoting the co-existence of conserva-
tive and acquisitive species. The co-existence of species with dif-
ferent strategies would lead to an increase in the functional trait
space at ridges, and consequently an increase in FRic. Similar val-
ues of functional structure across the other environmental gradi-
ents studied indicate that the variation and distribution of traits
within the trait space did not change (Carre~ no-Rocabado et al.
2012), although average trait values did change along the same
gradients. Consistent with these findings, Carre~ no-Rocabado et al.
(2012) showed that changes in FD indices were not as evident as
they were in CWM, as a response to disturbance in Bolivian trop-
ical forests.
The environmental gradients chosen in this study might not
be divergent enough to drive substantial changes in FD. Empha-
sizing the impact of traits measured, Magnago et al. (2014) dem-
onstrated a reduction in FEve and FDiv at forest edges in an
analysis of reproductive plant traits, however, traits related to
resource use, such as wood density, were not responsive to edge
effects in Brazilian Atlantic forests. Consistent with Magnago
et al. (2014), the lack of alterations in components of FD could
also change rapidly when the resilience or redundancy of present
species declines at the forest edges. A high species diversity and
turnover as in our study area (Lippok et al. 2013) could poten-
tially contribute to an increase in trait variation among and within
communities, and could buffer the effects of stress gradients on
the functional structure of these plant communities. Despite
ongoing human-induced land-use change, these Bolivian montane
forests might temporarily remain somewhat resilient.
Particularly with regard to FD, the choice of sampling design
as well as the suite of functional traits measured does affect the
outcomes of the investigation (Baraloto et al. 2010). Creating an
appropriate sampling design remains one of the biggest chal-
lenges in species-rich forests (Baraloto et al. 2010). We were
unable to measure functional traits of all species that occurred in
the plots; hence, values of functional composition and structure
refer to an incomplete data set. However, we sampled a combina-
tion of common species (60) following Garnier et al. (2004), and
less common species (59), considering the high number of spe-
cies with low abundance. Although a sampling design that
includes all species is ideal, we believe that combining traits of
common as well as less common species, together covering a
high percentage of species abundance, constitutes a reasonable
compromise for estimating community-level trait values.
456 Apaza-Quevedo, Lippok, Hensen, Schleuning, and Both
CONCLUSIONS
Overall, our results emphasize the intricate relationships between
functional leaf traits and physiological processes along complex
gradients of environmental conditions in tropical montane forests.
Varying soil conditions are the main driver of variability in leaf
traits in this montane forest. Accordingly, natural and human-
induced environmental gradients influenced soil properties and
were related to changes in functional composition of the woody
plant communities, indicating a conservative strategy of resource
acquisition in more stressful, nutrient-poor habitats, such as for-
est edges. The shift of CWM in leaf traits across elevation and
topography highlights the importance of natural gradients for
promoting variability in species traits and associated patterns of
species distribution and diversity in tropical montane forests.
Moreover, this study underscores the challenges of designing
sampling strategies in species-rich tropical forests.
ACKNOWLEDGMENTS
We thank Ricardo Sonco and Marcelo Reguerin for field assis-
tance, Arely Palabral and Heike Heklau for laboratory assistance
and the Herbario Nacional de Bolivia for the technical support.
We thank the community ‘Chulumani’ for their collaboration to
our research. This research was funded by the German Academic
Exchange Service (DAAD) and by the DFG project ‘Regenera-
tion of tropical mountain forest species at burned sites in the
Eastern Cordillera of Bolivia’ (HE3041/20-1). M.S. received the
research funding program Landes-Offensive zur Entwicklung
Wissenschaftlich-€okonomischer Exzellenz (LOEWE) of Hesse’s
Ministry of Higher Education, Research, and the Arts.
SUPPORTING INFORMATION
Additional Supporting Information may be found with online
material:
FIGURE S1. Schematic representation of the study design.
FIGURE S2. Rarefaction curves for 22 vegetation plots sam-
pled in a montane forest of Bolivia.
FIGURE S3. Representativeness of 119 species sampled for
the evaluation of six leaf traits in a montane forest of Bolivia.
FIGURE S4. Principal component analysis evaluating collinear-
ity of environmental variables.
FIGURE S5. Soil and microclimate variables along elevation,
topography, and edge effects in a montane forest of Bolivia.
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