Abundance and vigor of three selected understory species along environmental gradients in south-eastern Brazil
ABSTRACT The majority of floristic and phytosociological studies conducted in the Atlantic Forest are focused on tree species and tree species communities, while only limited research is done on understory species, in particular concerning their interrelationship with environmental factors or their ecological requirements in terms of habitat change due to anthropogenic influences, such as complete and selective logging. In our study, the species abundance and vigor of three representative species of the Atlantic Forest in south-eastern Brazil (Gesneriaceae: Nematanthus crassifolius, Besleria melancholica; Acanthaceae: Stenostephanus lobeliaeformis) were measured in a riverine ecosystem that included different levels of past logging activities along environmental gradients such as altitude, exposure, inclination, and canopy openness.
We measured the vigor of the species by counting the total number of shoots and estimating the rate of live shoots. To provide a comprehensive overview we developed a vigor index based on this data which might be useful for future studies on the response to environmental gradients of understory species in the tropics. The results show distinct relationships between various environmental factors and both species distribution patterns and vigor of the investigated species. N. crassifolius is strongly dependant on proximity to watercourses and open canopy conditions. Abundance of S. lobeliaeformis was limited to higher elevations, but according to our data individuals of this species are more vigorous at lower elevations of its distributional range. While being more vigorous with decreasing elevation, S. lobeliaeformis was completely absent at the lower end of the elevation gradient. The abrupt absence of this species at low elevations coincides with a complete forest clearance in the 1940s. S. lobeliaeformis was only found in the selectively logged forest. In contrast, changes in abiotic conditions have little effect on B. melancholica.
We conclude that small-scale elevational and microclimatic gradients have differing consequences for the selected understory species. Those natural gradients are disturbed by a land-use gradient, and a scenario like this is typical of the Atlantic Rainforest at this elevation. Therefore a further understanding, especially of the largely undersampled understory plant community, is essential and a first approach in this direction is provided by this study.
tural and floristic diversity is required for developing
conservation strategies (de Barcellos-Falkenberg &
Voltolini 1995, Metzger 1997, Morellato & Haddad
There is little information about the structure
and floristic composition of plant communities in
Neotropical montane forests (Madsen & Øllgaard
1994), particularly as regards changes in species
composition along altitudinal gradients within the
same geographic level (Cavelier 1996, Aiba & Kita-
yama 1999, Kessler 2001). Only a few studies on the
influence of small-scale altitudinal changes on com-
munities of trees, lianas, and herbaceous plants have
been carried out to date (Liebermann et al. 1985,
ECOTROPICA 16: 101–112, 2010
© Society for Tropical Ecology
ABUNDANCE AND VIGOR OF THREE SELECTED
UNDERSTORY SPECIES ALONG ENVIRONMENTAL GRADIENTS
IN SOUTH-EASTERN BRAZIL
André Lindner1, Katharina Stein2 & Martin Freiberg1,3
1Institute for Biology I – Department for Systematic Botany and Functional Biodiversity,
University of Leipzig, Johannisallee 21, 04103 Leipzig, Germany
2Institute for Geobotany and Botanical Garden, Martin-Luther-University Halle-Wittenberg,
Am Kirchtor 1, 06108 Halle, Germany
3Botanical Garden of the University of Leipzig, Linnéstrasse 1, 04103 Leipzig, Germany
Abstract. The majority of floristic and phytosociological studies conducted in the Atlantic Forest are focused on tree species
and tree species communities, while only limited research is done on understory species, in particular concerning their
interrelationship with environmental factors or their ecological requirements in terms of habitat change due to anthropo-
genic influences, such as complete and selective logging. In our study, the species abundance and vigor of three represen-
tative species of the Atlantic Forest in south-eastern Brazil (Gesneriaceae: Nematanthus crassifolius, Besleria melancholica;
Acanthaceae: Stenostephanus lobeliaeformis) were measured in a riverine ecosystem that included different levels of past
logging activities along environmental gradients such as altitude, exposure, inclination, and canopy openness. We measu-
red the vigor of the species by counting the total number of shoots and estimating the rate of live shoots. To provide a
comprehensive overview we developed a vigor index based on this data which might be useful for future studies on the
response to environmental gradients of understory species in the tropics. The results show distinct relationships between
various environmental factors and both species distribution patterns and vigor of the investigated species. N. crassifolius is
strongly dependant on proximity to watercourses and open canopy conditions. Abundance of S. lobeliaeformis was limited
to higher elevations, but according to our data individuals of this species are more vigorous at lower elevations of its dis-
tributional range. While being more vigorous with decreasing elevation, S. lobeliaeformis was completely absent at the
lower end of the elevation gradient. The abrupt absence of this species at low elevations coincides with a complete forest
clearance in the 1940s. S. lobeliaeformis was only found in the selectively logged forest. In contrast, changes in abiotic
conditions have little effect on B. melancholica. We conclude that small-scale elevational and microclimatic gradients have
differing consequences for the selected understory species. Those natural gradients are disturbed by a land-use gradient,
and a scenario like this is typical of the Atlantic Rainforest at this elevation. Therefore a further understanding, especially
of the largely undersampled understory plant community, is essential and a first approach in this direction is provided by
Key words: Acanthaceae, Atlantic Rainforest, distribution pattern, disturbance history, Gesneriaceae, vigor.
The Atlantic Rainforest (“Mata Atlântica”) is a highly
diverse ecosystem with an outstanding level of en-
demism (Fonseca 1985, Prance 1987, Morawetz &
Krügel 1997), but is currently threatened by ongoing
habitat loss and increasing forest fragmentation
(Ranta et al. 1998, da Silva & Tabarelli 2000, Oli-
veira-Filho & Fontes 2000, Tabarelli et al. 2005,
Ribeiro et al. 2009). The remaining remnants are a
mosaic of small, abiotically and biotically hetero-
geneous areas (Lima & Capobianco 1997, Gascon et
al. 1999). Comprehensive knowledge of their struc-
studied species. Additionally, this index might be a
useful tool to standardize the results and to enhance
the comparability of further studies.
The three studied species (Acanthaceae: Stenoste
phanus lobeliaeformis Nees; Gesneriaceae: Besleria
melancholica (Vell.) C.V. Morton, Nematanthus cras
sifolius (Schott) Wiehler) are typical understory her-
baceous plants of the coastal rainforest in the state of
Rio de Janeiro. The differences in their distribution
are presumably a result of habitat and microclimatic
heterogeneity. Thus we predict different require-
ments as regards environmental conditions for each
The main questions to be answered in our study
(1) Which environmental factors are related to the
abundance and vigor of the three species?
(2) How does the interdependency between environ-
mental gradients and the studied species change
in a forest with different historical and recent
Study area. The study was conducted from April to
September 2007 in the Atlantic Rainforest (“Mata
Atlântica”) of the state of Rio de Janeiro, Brazil in the
private reserve “Reserva Ecológica de Guapiaçu”
(REGUA – 22°25’53”S, 42°45’20”W) in the muni-
cipality of Cachoeiras de Macacu. The 5500-ha re-
serve is located on the south-facing slopes of the
Serra dos Órgãos Mountain range, about 100 km
from the city of Rio de Janeiro, and covers an alti-
tudinal gradient from 30 to 2200 m a.s.l. Most of
the mid- to high-elevation forests are protected at
State Park level. The mean annual temperature for
this region is about 23°C with a mean annual rainfall
of about 2560 mm. There is a hot and rainy season
from October to March and a cooler and drier season
from April to September (Kurtz & de Araújo 2000).
The vegetation can be classified as an evergreen
dense ombrophilous forest (Veloso et al. 1991) that
is typical for the lower and medium elevations of the
coastal mountain range (Morellato & Haddad 2000,
Oliveira-Filho & Fontes 2000). Due to forest logging
for agriculture on the property of REGUA since the
beginning of the 20th century (Locke, pers. comm.)
there are now vegetation formations of several suc-
cession stages. The oldest parts of the regrown forest
are mostly connected to the continuous forest of the
mountain range and are now turning into mature
Horvitz & Le Corff 1993, Freiberg & Gottsberger
The local climate plus environmental and/or
historical factors are the main elements determining
species composition in tropical rainforests on a re-
gional scale (Webb 1968, Whitmore 1973, Hall &
Swaine 1976), but there exists a hierarchy of different
influences within a given climatic region. The frag-
mented Atlantic Rainforest is a mosaic of different
disturbance scenarios, showing a complex history of
logging events of varying degrees. The interdepen-
dence between such anthropogenic impacts and the
requirements of the vegetation is of great interest
when attempting to understand the ecological con-
sequences at the species level.
Most of the published results of floristic and
phytosociologic studies in south-eastern Brazil focus
on woody plants forming the canopy layer (Andrea-
ta et al. 1997). Nevertheless, herbaceous plants of the
understory contribute significantly to species richness
in tropical plant communities, representing 20-50%
of the local diversity of vascular plants (Gentry &
Dodson 1987, Gentry & Emmons 1987, Andreata
et al. 1997, Duque et al. 2002). However, there is a
lack of knowledge about limiting factors and the key
influences of environmental gradients on the abun-
dance, vigor, and growth of understory species (Lie-
bermann et al. 1985, Freiberg 1994, Freiberg &
Gottsberger 2001, Drucker et al. 2008).
We examined the relationship between poten-
tially key environmental factors, such as elevation,
inclination, exposure, distance to river, and canopy
openness, and individual species performance. Each
of those parameters is a describing variable for mi-
croclimatic conditions affecting the understory plant
community. Lopes et al. (2005) identified numerous
microhabitats in the Atlantic Rainforest that are
essential to the diversity of understory species, given
the heterogeneity of local topography and environ-
mental conditions. Our study continues this work
and extends our knowledge of the response of species
to environmental gradients.
Besides gaining knowledge of the ecology of
understory plants it is important to evaluate the in-
fluence of differing disturbance history, in terms of
logging, in varying dimensions. It remains uncertain
to which degree each of those components relates to
the understory community.
We developed a vigor-index, based on growth
variables, to quantify the health conditions of the
LINDNER ET AL.
of Rio de Janeiro. It grows around the city of Rio de
Janeiro and in the Serra dos Õrgãos at elevations of
between 150 and 1200 m a.s.l. The genus is common
in the understory of pluvial forests in shady habitats
near slopes and waysides (Lopes et al. 2005, Kriebel-
In the Neotropics the genus is one of the most
diverse genera within the Gesneriaceae, comprising
about 160 species, at least 16 of them occurring in
Brazil (Chautems 1991 and pers. comm.).
Nematanthus crassifolius (Schott) Wiehler (Gesne-
N. crassifolius is an obligate epiphytic or accidentally
epilithic species (Chautems 1988). The climbing or
pendulous shoots are slightly lignified and hairless.
This species is endemic to the Atlantic rainforest of
south-eastern Brazil (Lopes et al. 2005) and has been
recorded in the states of Espírito Santo, Minas Ge-
rais, Rio de Janeiro, and São Paulo growing at ele-
vations of between 50 and 1500 a.s.l. (Chautems
and Kiyama 2003, Chautems, pers. comm..). The
pubescent and oval-elliptical leaves are anisophyllous
with green glossy upper surface, whereas the under-
side is infrequently red-magenta in color. This va-
riance is interpreted as an ecotype (Blanc 2002).
N. crassifolius is frequently found near riversides
and occurs sometimes as isolated individuals in the
forest interior (Lopes et al. 2005).
Study design. Starting about 100 m downriver of a
waterfall we established six transects along the Rio
Manuel Alexandre. Each transect was 100 m in
length and 10 m wide, separated into two 50-m
subtransects on each side of the river at right angles
to its course (Hoagland & Collins 1997). Each sub-
transect was divided into five plots of 10 m x 10 m
each (Annaselvam & Parthasarathy 2001, Freiberg &
Gottsberger 2001), resulting in a total of 0.1 ha for
every transect. They were located within a minimum
distance of 250 m (along the course of the river) of
each other. During the establishment of these
transects, tributaries were avoided and the accessibi-
lity of the waterside was taken into consideration to
prevent a disarrangement of the transect line (Fernán-
dez-Aláez et al. 2005). The three upper transects
(400-320 m a.s.l.) were situated in a forest formation
where selective logging took place until the 1970s,
whereas the other three transects at a lower elevation
(250-200 m a.s.l.) were located within forest which
was completely felled around the 1940s (Locke, pers.
comm.) (Fig. 1).
forest. In the lower parts of REGUA, and within the
areas used as pasture and agricultural land, the forest
is highly fragmented and disturbed.
Study species. We selected three understory species
which are common in the study area and easy to
recognize (Acanthaceae: Stenostephanus lobeliaeformis
Nees, Gesneriaceae: Besleria melancholica (Vell.) C.V.
Morton; Nematanthus crassifolius (Schott) Wiehler).
Species of the family Acanthaceae grow in diverse
habitats like forests, swamps, or pastures. Because of
the species richness within this family (app. 85 gene-
ra and 2000 known species in the Neotropics) there
is a huge lack of knowledge about the distribution,
endemism, and ecological requirements of individu-
al species (Wasshausen 2005).
Stenostephanus lobeliaeformis Nees (Acanthaceae):
This species is an erect perennial woody herb and
grows as a ramified sub-shrub with a height of up to
1.50 m. The genus contains about 39 species which
are common within cloud forests, along riversides
and in wet dips (Daniel 1999). Its distribution is
exclusively neotropical and ranges from southern
North America to Colombia and Brazil. S. lobeliae
formis is listed as a vulnerable species in the state of
Espirito Santo in Brazil.
The family of Gesneriaceae is a useful indicator
group in vegetation classification studies in the trop-
ics according to criteria like specialization of individ-
ual species to habitat and easy recognition in the field
(Kessler & Bach 1999). Many species are endemic to
geographically small areas or, the majority, restricted
to specific habitats (Denham 2004) and generally
disappear when habitats face sustained disturbance.
They can be regarded as indicators for the diversity
of flowering plants and as representatives of the status
of the whole flora of a given area (Skog 2005).
The life forms of the common genera Besleria and
Nematanthus are species-specific as well as habitat-
dependent. They appear as herbs, sub-shrubs or
shrubs and grow terrestrially, hemiepiphytically, or
epiphytically. Those life forms show different require-
ments regarding abiotic factors like light intensity,
humidity, and soil characteristics (Lopes et al. 2005).
Besleria melancholica (Vell.) C.V. Morton (Gesne-
The genus Besleria is one of only a few genera of
Gesneriaceae whose species grow as shrubs or even
small trees. Besleria melancholica is a perennial shrub
endemic to the coastal Atlantic rainforest of the state
ABUNDANCE AND VIGOR IN UNDERSTOREY
LINDNER ET AL.
FIG. 1. Location of the research transects along the Rio Manuel Alexandre within the area of the “Reserva
Ecológica de Guapiaçu” (REGUA – 22°25’53”S, 42°45’20”W) including the elevation profile of the river
course and the logging activities in the forest. (Aerial photograph source: Mr. Nicholas Locke, REGUA).
ShLInd number of living shoots on individual plant
ShTInd total number of shoots on individual plant
ShBInd number of living shoots in large size class
ShMPop maximum number of living shoots per in-
dividual in the investigated population
V vigor-index score
The index ranges from 0 to 1 with the higher-
scoring individuals being more vigorous. The peak
value of 1 is reached for an individual with the
maximum number of shoots in the whole investi-
gated population, all of them alive and in the large
size class, whereas a value of 0 indicates an individ ual
without any living shoots.
Statistical analysis. Because of the division of 100-m
transects into 10 plots of 10 x 10 m each, the in-
dividual plots are located side by side. Thus the sta-
tistical treatment of those areas as independent units
might be questionable in terms of the effect of spa-
tial autocorrelation (e.g. Legendre 1993, Diniz-Filho
et al. 2008). There are two commonly used indices
to test for spatial autocorrelation. Moran’s I (Moran
1950) is a measure of global spatial autocorrelation,
while Geary’s C (Geary 1954) is more sensitive to
local spatial autocorrelation and was used in this
case. Geary’s C was calculated using ROOKCASE
In every plot the following abiotic parameters
were measured: altitude, distance to river, inclination
and exposition, as well as canopy openness. Altitude
was measured with a barometric altimeter (SuuntoTM
Vector) and distance to the river was determined by
measuring tape. To obtain inclination data we made
an inclinometer out of a simple 180° protractor by
fixing a plumb line at 90°, which referred to zero
degree inclination. By holding the inclinometer
parallel to the slope we measured the inclination.
Exposition was measured with a standard compass.
To use exposition as an analyzable environmental
factor it was transformed into a non-circular variab-
le by calculating the sinus of the exposure degrees,
whereby exposure is denoted as “easternness”. Can-
opy openness was measured by taking hemispherical
photographs at the center of each 10 x 10-m plot.
We used a Nikon Coolpix 4500 digital camera in
combination with a Nikon FC-E8 fisheye-lens. Re-
solution was set to 2272 x 1704 pixels. The camera
was fixed on a tripod 1.30 m above the ground,
leveled and looking upwards to the sky. Pictures
were only taken under overcast conditions to avoid
overexposure and to reduce reflections on leaves
which could be construed as openings (Trichon et al.
1998, Williams et al. 2003). The WinScanopy
2005ab software (Regent Instruments Inc. 2005) was
used to analyze the hemispherical photographs and
to derive canopy openness data. Canopy openness is
defined as the proportion of open sky area in a 180°
hemisphere monitored from a central point. Pixels of
digital images are to be classified as either “canopy”
or “sky” based on the grayscale value (pictures are
automatically transformed to grayscale from color
photographs by the software).
Abundance and vigor of all individuals of the
investigated species were recorded. All individuals of
all three species were counted in every plot per
transect. The total number of shoots, and the number
of living ones, was acquired per plant individual.
Living shoots were estimated in length and classified
into two size classes (small 0-60 cm, large > 60 cm).
This method was chosen because most individuals of
N. crassifolius were growing as epiphytes and therefore
were situated out of reach for exact measurements.
Using shoots as a morphological trait for vigor esti-
mation in tropical understory plants is an established
method (Bruna et al. 2002)
The following characteristics were selected as
indicators of vigor and combined into a vigor-index
for every individual:
ABUNDANCE AND VIGOR IN UNDERSTOREY
V = ShLInd
ShTInd + 1
N number of observations
i,j location within transect (plot)
X variable of interest (abundance of species, canopy
ωij distance (spatial lag) between locations i and j
W sum of all ωij
The value of Geary’s C lies between 0 and 2.
Geary’s C approaches 1 when the spatial pattern is
close to random, and it is less than or greater than 1
when the spatial pattern is respectively clustered or
We tested for spatial autocorrelation in distri-
bution of the studied species and environmental
variables (canopy openness and inclination). Para-
(N–1) ∑i ∑j ωij (Xi–Xj)2
2W ∑i (Xi–X–)2
species data we used two consecutive approaches.
In a separate model, environmental variables were
treated individually, whereas variables were added
sequentially into the model using a forward selection
model (Monte Carlo permutation test with 1000
permutations under full model). Permutation restric-
tions were set to split-plot design (linear transect).
To extract the weight of single environmental
factors, and to examine their relationship to the
abundance of each species separately on the one hand
and to the vigor-index score V on the other, we used
multiple regression analyses, including stepwise for-
ward procedures to exclude possible co-interactions.
To test for differences in canopy openness in
transects within the two areas of differing disturbance
history we used a Kruskall-Wallis one-way analysis of
variance (ANOVA) on ranks including a Student-
Newmann-Keuls all pairwise multiple comparison
Altogether we found 301 individuals of S. lobeliae
formis, 175 of N. crassifolius (including five individ-
uals of the red-magenta-colored ecotype), and 75
individuals of B. melancholica, giving a total of 551
individuals of all investigated species in all transects
covering a total area of 6000 m².
S. lobeliaeformis was most abundant in the upper
transects (e.g. 65% of all individuals in T2 and T3),
whereas abruptly in T4 only one individual was
found, while in the lowest transects T5 and T6
the species was completely absent. B. melancholica
showed a similar distribution pattern and was only
present in higher elevations (T1, T2, and T3), with
the highest number of individuals in the uppermost
transect. N. crassifolius was concentrated in the lower
regions (T4, T5, and T6) with only few individuals
(including all five individuals of the red-magenta-
colored ecotype) found at a higher elevation (T1 and
meters with a direct spatial reference (distance to river
and exposition) were excluded from the analysis. In
the majority of cases the results show a distribution
close to a random spatial pattern (Table 1), with the
exception of environmental variables in T6 because
of the almost complete clearing of the steep eastern
part of this particular transect.
The outcome of the spatial autocorrelation ana-
lysis of our data indicates a general random spatial
pattern of the variables at the given scale and there-
fore plots can be statistically treated as independent
To check on redundant information within the
environmental variables we additionally used the
nonparametric Spearman Rank Order Correlation.
Only a single significant correlation was detected
between canopy openness and elevation. Although
the relation between both factors is not exceptio nally
strong (r = -0.437, P < 0.001) it has to be kept in
mind when interpreting further results.
To examine if the species distribution was related
to the environmental variables we performed a re-
dun dancy analysis (RDA) using the CANOCO 4.5
software package, following Lepš and Šmilauer
(2003). First a detrended correspondence analysis
(DCA) was carried out on species distribution data
only. The longest gradient was 2.35 SD (SD = stan-
dard deviation of units of species turnover), and
therefore the species respond roughly linearly to
gradients. Thus RDA was used following Lepš and
Šmilauer (2003) for gradients less than 3 SD instead
of CCA (canonical correspondence analysis), which
is the appropriate model for a unimodal response.
RDA was carried out with a focus on inter-species
correlation. Species scores were divided by the
standard deviation. Additionally, species abundance
data were log-transformed to prevent high values
influencing the ordination. To evaluate environmen-
tal variables in their importance for determining
LINDNER ET AL.
TABLE 1. Geary’s C (local spatial autocorrelation) for species distribution and data apportionment of non-
spatial environmental factors in all transects.
Geary’s C T1 T2 T3 T4 T5 T6 mean
1 value in parentheses excluding T6
mis, but the overall regression model is rather weak
(R² = 0.1). Elevation had more influence on the
abundance of B. melancholica, which was additio nally
affected by inclination. Both factors significantly
contributed to the multiple regression model (R² =
0.26). N. crassifolius was almost exclusively found
within proximate riparian vegetation. Therefore dis-
tance to the river was a crucial factor in N. crassifo lius,
whose abundance shows a negative correlation with
this single parameter contributing to the multiple
regression model (R² = 0.23). Neither canopy
openness nor exposition had a detectable influence
on the occurrence of the studied species (Table 2).
The effects of different environmental factors on
vigor (using the vigor-index) also showed varying
patterns between the species (Table 3). S. lobeliae
formis was the most sensitive species in terms of
susceptibility to environmental influences. We ob-
served a significant negative correlation with eleva-
Distribution of all three species was explained
mainly by elevation (F = 12.48, P < 0.001) and
distance to river (F = 11.65, P < 0.001). We found
minor and barely significant effects for inclination
(F = 3.01, P = 0.052) and canopy openness (F = 1.83,
P = 0.227). Altogether these four variables of the
forward selection model explained 38% of the com-
plete variance in species distribution. Exposure was
completely excluded due to the lack of any contribu-
tion to the model.
The ordination diagram emphasizes the consid-
er able effects of the distance to the river in N. crassi
folius as well as the influence of elevation on S. lobe
liaeformis and B. melancholica within this model (Fig.
The effect on abundance of various environmen-
tal factors differs between the investigated species
(Table 2). Elevation was the only parameter signi-
ficantly influencing the abundance of S. lobeliaefor
ABUNDANCE AND VIGOR IN UNDERSTOREY
FIG. 2. RDA ordination diagram including all three species (Steno – Stenostephanus lobeliaeformis, Besl –
Besleria melancholica, Nem – Nematanthus crassifolius; species fit range: 25-100%) and four environmental
variables (elev – elevation, dist – distance to river, incl – inclination, and co – canopy openness).
The diagram indicates open habitats at low elevation near the river bank for N. crassifolius and more closed
canopy conditions at higher elevation for S. lobeliaeformis and B. melancholica, both being more in dependent
of proximity to the watercourse.
gradients. Therefore more qualitative information on
ecological requirements and logging disturbances
should be obtained.
S. lobeliaeformis and B. melancholica are abundant
in transects at the higher elevation and completely
absent in the two lowest ones, whereas N. crassifolius
is common in this lower region only. The complete
altitudinal gradient amounts to only 207 m, and is
completely situated in the submontane level within
a forest formation subjected to differing extents of
logging activity in the past. There are considerable
relationships between environmental gradients and
both abundance and vigor of the studied species
within such a small-scale region. Similar results have
been published for Cyclanthaceae (Freiberg & Gotts-
berger 2001), for other herbaceous plants (Horvitz
& Le Corff 1993), as well as for lianas and trees
(Liebermann et al. 1985).
N. crassifolius occurs mainly in the lower part of
the research area and almost exclusively directly by
the river. This confirms the observations of Lopes et
al. (2005). Epiphytes have no access to soil water and
rely on air humidity and precipitation. The humus
layer on the phorophyte can provide limited water
resources, but epiphytic species can fall back only on
tion and a positive one with canopy openness relating
to the vigor of this species, resulting in a multiple
regression coefficient of R² = 0.36. In contrast, B.
melancholica was very robust regarding the influence
of the environmental gradients on vigor. There was
no significant effect of any tested parameter at all in
this species. The vigor of the epiphytic N. crassifolius
showed a significant positive response to canopy
openness only, but overall the regression model was
weak (R² = 0.05).
Canopy structure between the upper (T1, T2,
and T3) and lower transects (T4, T5, and T6) dif-
fered: canopy openness in the lower transects within
the formerly clear-cut area is significantly higher than
in the upper transects within the area where selective
logging took place (Table 4).
The distribution of the chosen species in this study
is mainly influenced by elevation and distance to the
river. Both factors stand for variation in microcli-
matic habitat conditions (temperature, wind, and
evapotranspiration). Vigor data of understory plants
based on growth variables seem to be more sensitive
and responsive to such small-scale environmental
LINDNER ET AL.
TABLE 2. Results of a multiple regression analysis (stepwise forward) with influence of environmental vari-
ables on abundance.
std. coeff. R F P R F P R F P
distance to river
0.474 16.514 <0.001
0.312 0.312 6.146 0.016 0.408 0.445 12.382 <0.001
- 0.754 0.389 0.259 0.514 4.984
TABLE 3. Results of a multiple regression analysis (stepwise forward) with influence of environmental vari-
ables on vigor-index score.
std. coeff. R F P R F P R F P
distance to river
0.226 0.352 9.669 0.002
-0.460 0.309 40.016 <0.001
1.205 0.234 0.227 0.227 9.184 0.003
-1.107 0.274 -
-0.242 0.810 -
0.472 0.639 -
-0.574 0.569 -
2.807 0.0960.363 0.548
microhabitats. Even small-scale topographic diffe-
rences influence edaphic and hydrological condi-
tions, leading to such habitat diversity (Austin &
Greig-Smith 1968, Williams et al. 1969, Hall and
Swaine 1981). The genus Besleria is known to be
common on steep slopes at medium elevations in the
Atlantic Forest (Lopes et al. 2005, Chautems, pers.
comm.), which was confirmed for B. melancholica in
this study by the positive relationship between abun-
dance and elevation as well as inclination. Steep
slopes are well aerated via lateral runoff, whereas
water accumulates in hollows. B. melancholica seems
to rely on well-drained soils for establishment and
represents an example of the influence of complex
microtopographical gradients on species distribution
within heterogeneous microhabitats (Webb 1968).
Regarding to our study B. melancholica is a generalist
species, underlined by the evidence of no significant
effects on the vigor performance (Table 3).
On the other hand more substantial effects were
recorded for S. lobeliaeformis. We registered an abrupt
disappearance of S. lobeliaeformis after a constant
increase in vigor performance with decreasing eleva-
tion. This inconsistent finding may be caused by the
different disturbance history in this region (Fig. 3).
The borderline of the range of S. lobeliaeformis is
consistent with this pattern. In the lower part of this
area where clear-cutting took place in the 1940s the
species is completely absent, whereas in the upper
region only selective logging was conducted before
the 1970s (Locke, pers. comm.). It is presumed that
S. lobeliaeformis normally occurs in the lower area
and performs better there than in higher regions. The
responsible factor could not be isolated but it seems
certain that there is some kind of distribution barrier
for S. lobeliaeformis which might be due to the dif-
ferent disturbance history. The antithetical finding
of increasing abundance with increasing elevation
(Table 2) can be neutralized by removing all plots
with no individuals of S. lobeliaeformis or removing
all plots with a history of severe logging from the
analysis. After both modifications no environmental
parameter has any significant influence on the abun-
dance of that species. A prospective approach on a
larger scale, including the extension of the altitudinal
gradient, could be helpful at this point. Another
indication for the hypothesis that S. lobeliaeformis
responds to modified conditions according to dif-
fering logging impact is the different forest structure.
Canopy openness of the lower transects within the
former clear-cutting area is significantly higher than
in the upper transects within the area where selective
water stored within their own plant body if such
sources are depleted (Freiberg 2000, Freiberg &
Gottsberger 2001). Therefore N. crassifolius depends
on habitats with adequate air humidity. In addition,
pollination and dispersal may be explanations for the
population structure of N. crassifolius. Pollination
rates are possibly higher along the riverbanks, given
the accumulation of individuals and a better acces-
sibility for pollinators. Based on the flowering pattern
it is probable that hummingbirds are the main pol-
lination agents. Higher pollination rates go along
with higher fructification rates. The fruits of N. cras
si folius are fleshy capsules and dispersal by birds is
likely. Birds mostly prefer open corridors like rivers
and defecate in the immediate vicinity (Charles-
Dominique 1986), resulting in a concentration of
N. crassifolius near riversides and isolated individuals
within the forest interior (Lopes et al. 2005). There
is no empirical information about any causality
between reproduction rate, seed dispersal, and pop-
ulation structure in N. crassifolius, therefore any ar-
gumentation is hypothetical.
The vigor performance of N. crassifolius shows a
significant but rather weak positive correlation with
canopy openness (Table 3). Light availability is
known to be the main determinant of the vertical
distribution of epiphytes on host trees (Wolf 1994)
and might be an important parameter here. But if air
humidity is at a constantly high level, relative irra-
diance is only a secondary limiting factor for growing
S. lobeliaeformis and B. melancholica occur syn-
topically in the upper transects. Nevertheless they
were barely found together within the same plot. It
is expected that both species have similar habitat
requirements, but avoid strong competition by using
different niches provided by the multifarious riverine
ABUNDANCE AND VIGOR IN UNDERSTOREY
TABLE 4. Results of a Kruskall-Wallis one-way
ANOVA on ranks including a Student-Newmann-
Keuls all pairwise multiple comparison procedure of
canopy openness conditions in two forest formations
with different disturbance history.
group N median 25% 75%
H = 12.909; df = 1; P < 0.001
selective logging vs. clear-cutting: diff of ranks = 486;
q = 5.081; P < 0.05
might be useful as an indication tool for management
issues in areas with different disturbance histories.
The vigor-index introduced within our study has
been proved helpful for detecting growth responses
due to changing environmental conditions. Biomass
could also be an appropriate factor to ascertain the
level of vigor (Freiberg & Gottsberger 2001), but
lacks the advantage of being non-destructive.
We are grateful to the “Reserva Ecológica de Guapia-
çu” (REGUA) and the whole staff, especially to Mr.
Nicholas Locke, for logistical support and the per-
mission to work on the property. We would like to
thank Alain Chautems and an anonymous reviewer
for helpful comments on the manuscript. For field
assistance we would like to thank Corinna Burkart
and Maria Faske, as well as Dietmar Sattler for valu-
able help in preparing this study and providing
mobility backup in arduous conditions. We are
grateful to the University of Leipzig and the German
Academic Exchange Service (DAAD) for funding.
logging took place (Table 4), and canopy openness
was identified as positively influencing the vigor of
S. lobeliaeformis as well (Table 3). But this finding
has to be accepted with reservations because of the
co-correlation between canopy openness and eleva-
tion (r = -0.437, P < 0.001) and the location of the
areas with different disturbance histories at different
altitudinal levels. Thus we cannot certainly distin-
guish between the influence of elevation and histori-
cal use of the area.
Although this study only deals with three re-
presentative understory species, in summary the in-
fluence of complex environmental gradients on abun-
dance and vigor is observable, even on a small-scale
level. Apparently there are differences within a small
altitudinal range and within the same vegetation
formation and our results may be applicable to the
whole understory community (Drucker et al. 2008).
Apart from the different ecological requirements of
the species, a potential impact of past logging acti-
vities on abundance and vigor cannot be denied.
Generally the high sensibility of certain species to
environmental changes due to land use activities
LINDNER ET AL.
FIG. 3. Significant trend in decrease of vigor in Stenostephanus lobeliaeformis with increasing elevation. The
species was found only in the three upper transects and was absent in the lower ones. The distribution pattern
agrees with the range of different logging activities of the particular areas.
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