Landscape and Urban Planning 120 (2013) 107–118
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Landscape and Urban Planning
journal homepage: www.elsevier.com/locate/landurbplan
Research paper
Using high-resolution remote sensing data for habitat suitability
models of Bromeliaceae in the city of Mérida, Venezuela
Caroline Judith a,b,∗ , Julio V. Schneider a,b,c , Marco Schmidt a,b,c , Rengifo Ortega d ,
Juan Gaviria e,f , Georg Zizka a,b,c
a
Senckenberg Research Institute and Natural History Museum Frankfurt, Department of Botany and Molecular Evolution, Senckenberganlage 25, 60325
Frankfurt am Main, Germany
b
Goethe-University, Institute of Ecology, Evolution and Diversity, Max-von-Laue-Str. 13, 60439 Frankfurt am Main, Germany
c
Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, 60325 Frankfurt am Main, Germany
d
Geomatikk AS, Oslo Section, Postbox 103, Økern, Norway
e
Instituto Jardín Botánico, Facultad de Ciencias, Núcleo La Hechicera, Universidad de los Andes, Apartado 52, 5212 Mérida, Venezuela
f
GeoBio-Center LMU, Ludwig-Maximilians-University München, Richard-Wagner-Str. 10, 80333 München, Germany
h i g h l i g h t s
• Twenty species and four genera of Bromeliaceae were found in the city of Mérida.
• Bromeliaceae differ in their ecological preferences, with CAM species being adapted to sealed areas.
• Combining satellite and elevation data is suitable for bromeliad distribution models.
a r t i c l e
i n f o
Article history:
Received 24 October 2012
Received in revised form 26 April 2013
Accepted 19 August 2013
Keywords:
Andes
Bromeliaceae
Habitat suitability modelling
Satellite imagery
Tillandsia
Urban biodiversity
a b s t r a c t
Little information is available concerning the effects of the increasing urbanization on biodiversity in
tropical regions. Species distribution modelling based on interpolated climate data is a widely applied,
time- and cost-effective tool to estimate the potential species richness in a target area. However, high
fragmentation, strong environmental gradients on a small-scale, and lack of fine-scale environmental data
in tropical urban areas require alternative approaches. In this study we combined a rapid species assessment approach with environmental niche modelling based on high-resolution ASTER satellite imagery to
predict species distributions of Bromeliaceae in the city of Mérida, Venezuela. Twenty species of Bromeliaceae, e.g. 36% of the total bromeliad diversity of the state of Mérida, were observed in the city, including
seven species with CAM physiology. CAM species showed significantly higher occurrence probabilities in
zones with higher soil sealing, whereas in C3 species a trend across soilsealing zones was not observed.
The remarkable urban species richness of Bromeliaceae is here attributed to the species’ different adaptive strategies, as well as to the strong elevation gradient of Mérida city. Our species modelling approach
provides new possibilities for the identification of indicator species in different urban built-up areas.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Urbanization continues to increase on a global scale and
individual cities are attaining unprecedented sizes. Nowadays,
more than 50% of the world’s population lives in urban areas
∗ Corresponding author at: Goethe-University, Institute of Ecology, Evolution and
Diversity, Max-von-Laue-Str. 13, 60439 Frankfurt am Main, Germany.
Tel.: +49 069 798 42226.
E-mail addresses: caroline.judith@ymail.com (C. Judith),
Julio.Schneider@senckenberg.de (J.V. Schneider), Marco.Schmidt@senckenberg.de
(M. Schmidt), rengifo.ortega@geomatikk.no (R. Ortega), gaviria@ula.de (J. Gaviria),
Georg.Zizka@senckenberg.de (G. Zizka).
0169-2046/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.landurbplan.2013.08.012
(United Nations, 2010). This trend imposes severe pressure upon
the biodiversity in urban areas, making biodiversity research in
populated areas a major concern. For historical reasons, most ecological and biodiversity assessments in urban areas have been
conducted in industrialized countries of the northern hemisphere,
whereas few studies are known from tropical or subtropical major
cities (e.g. Franceschi, 1996; Sattler, Schmidt, & da Silva Alves,
2010), many of which are among the fastest growing ones worldwide (Cohen, 2006).
Urbanization is accompanied by a multitude of effects on the
local species composition, such as habitat loss, fragmentation, isolation, and alteration. Generally, urban areas are characterized by
highly fragmented green areas with different levels of connectivity
108
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
and altered environmental conditions (Antrop, 2000; McKinney,
2002). Permanently changing conditions require specific adaptation of species for survival. It is therefore of particular interest
for conservation and planning issues to understand the potential
distribution of species in such an extreme habitat.
In recent years, habitat suitability models (HSMs; or similar
models like ecological niche models, environmental niche models,
species distribution models) have become increasingly important
for studying species distribution patterns. The general purpose of
these modelling approaches is to estimate the potential geographic
species distribution by considering the ecological requirements
that are suitable for a species’ occurrence (Guisan & Zimmermann,
2000). This procedure diminishes misinterpretations made by
traditional techniques, like point-occurrence maps (Hijmans &
Graham, 2006). However, this technique is rather underrepresented in the field of urban biodiversity research. Developments
in geographic information systems (GIS), terrain modelling, and
climate data interpolation techniques have led to more precise
environmental niche models (Elith et al., 2006; Franklin et al.,
2013; Kriticos et al., 2012; Seguardo & Araújo, 2004). Until now,
resource direct and indirect environmental gradients in terms of
raster climate data sets and digital elevation models (DEM) were
mainly used as input data during modelling. A major drawback
of raster climate data and DEM is that fine-scale environmental
data are usually not available for the species-rich tropical countries
(Soria-Auza et al., 2010). In contrast, satellite data are widely
available. Due to the direct measurement of the earth surface,
these data provide spatially refined information of landscape and
hydrological characteristics. Consequently, fine-scale habitat heterogeneity, as is observed in urban areas, is adequately represented
and their incorporation in HSMs opens new opportunities. The
successful application of satellite data has been shown in various
ecological investigations of different taxonomic groups (Buermann
et al., 2008; Morán-Ordóñez, Suárez-Seoane, Elith, Leonor, & de
Estanislao, 2012; Schmidt, König, & Müller, 2008; Zimmermann,
Edwards, Moisen, Frescino, & Blackard, 2007). However, to our
knowledge no modelling of the habitat suitability of vascular plant
species in urban habitats using satellite data has been conducted
to date.
In this study, the family Bromeliaceae is used as an example
for modelling species distributions in a neotropical urban area.
Bromeliaceae is one of the largest monocot families, comprising
58 genera and 3248 species (Luther, 2010), and is the second
most important family of neotropical epiphytic phanerogams in
terms of species numbers after the Orchidaceae (Benzing, 1990;
Gentry & Dodson, 1987). They are exclusively neotropical with
the West African Pitcairnia feliciana being the only exception. The
family includes terrestrial species as well as extreme epiphytes.
Due to numerous morphological and physiological adaptations, like
leaf succulence, crassulacean acid metabolism (CAM), and specialized water-absorbing trichomes, bromeliads successfully colonize
a broad range of natural habitats including rain forests, savannahs,
deserts, and rocks. Tank bromeliads, species that impound water
due to their tight leaf bases, provide aquatic habitats for a large
number of animals, including arthropods and amphibians, thus
contributing to the total biodiversity. Noteworthy is that bromeliads are either obligate C3 plants or facultative to obligate CAM
plants (Martin, 1994), with the latter being characterized by a
higher drought tolerance which in turn might be advantageous for
successfully colonizing the generally drier urban areas.
Thus, the diversity displayed by bromeliads and their ability to
colonize different habitats makes them an excellent model plant
family for the study of ecological niches in neotropical urban environments. Additionally, they may serve as surrogate taxa for urban
species diversity because many species are widespread, occurring in large parts of the Neotropics. Numerous studies have been
conducted regarding diversity and distribution patterns of bromeliads in their natural or semi-natural habitats (e.g. Hornung, 1998;
Krömer, Kessler, & Gradstein, 2007; Schneider, Gaviria, & Zizka,
2003; Zizka et al., 2009). However, their distribution in urban habitats is largely unknown.
The aims of this study are (1) to examine the diversity of
Bromeliaceae in a tropical urban area and their distribution among
urban habitats, (2) to test whether CAM bromeliads are more successful in colonizing urban areas than C3 bromeliads, (3) to evaluate
the utility of high resolution satellite images for habitat suitability
modelling in highly fragmented urban areas.
2. Materials and methods
2.1. Study site
The study site encompasses the city of Mérida (Mérida state,
Venezuela) as displayed by the official city boundary designated in
the map “Plan de desarrollo urbano local de Mérida, marco de referencia” (Universidad de Los Andes, Facultad de Arquitectura y Arte,
Unidad de Consultoría Externa y Proyectos). The city is located at
a mean elevation of 1630 m a.s.l. (1000–2400 m) on a quaternary
plateau in the Venezuelan Andes flanked by two mountain ranges,
the Sierra Nevada to the east and the Sierra de la Culata to the northwest. Mérida has approximately 230,000 inhabitants and covers an
area of 55 km2 . The climate is tropical mountainous. The precipitation has a bimodal annual distribution, with peaks in May–June
and September–November, and the mean annual precipitation is
1737 mm (Stansell, Polissar, & Abbott, 2007). The mean annual
temperature is between 16 and 20 ◦ C (Foghin-Pillin, 2002; Rojas &
Alfaro, 2000) and is typical of low latitudes, showing strong diurnal
oscillations but little seasonal variability. The main watercourses of
Mérida are the Río Chama and the Río Albarregas. The city is located
in an area of the lower montane rainforest (sensu Kappelle, 1996),
but most of the original vegetation has been transformed and only
small remnants of the forests currently persist within the limits
of the city. The surrounding montane rainforests are characterized
by tree species of genera such as Billia (Hippocastanaceae), Brunellia (Brunelliaceae), Weinmannia (Cunoniaceae), Clusia (Clusiaceae),
and Decussocarpus (Podocarpaceae), accompanied by abundant
epiphytes of the families Bromeliaceae, Orchidaceae, and Piperaceae (Engwald, 1999; Kelly, Tanner, Lughadha, & Kapos, 1994;
Schneider, 2001; Schneider et al., 2003).
The suburbs to the North, East, and West are built into the mountain slopes and are therefore situated at higher altitudes than the
city center, which is located in the stream’s channel. These outskirts are characterized by a lower population density, and contain
more semi-natural environments, such as house gardens and areas
with typical ruderal components, as well as natural sites. Besides
building areas, Mérida includes also sectors of used and abandoned
agricultural land and forest fragments. All identified land cover
classes are listed in Table 1.
2.2. Sampling design and botanical collections
In order to assess the species diversity of bromeliads across the
different urban habitat types, species occurrences were recorded
within 79 representative plots (Fig. 1). These study plots were
selected using an ASTER satellite image combined with a roadmap,
and are equally distributed among the various built-up classes,
vegetation types, and altitudinal zones of the city. Only study plots
with at least one species occurrence were taken into consideration,
in accordance with the requirements for the HSM technique (see
below). Inaccessibility of the terrain restricted the number of
plots between 1000 and 1200 m, and between 2000 and 2200 m.
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
109
Table 1
System of grouped land cover classes to urban zones of Mérida city according to the degree of soil sealing.
Zone
Soil sealing (%)
Relative area in
Mérida city (%)
Land cover classes
1
2
75–100
50–74.9
22
36
3
4
25–49.9
5–24.9
6
17
5
0–4.9
19
Core area, city center; streets (paved); bare, highly impervious compacted soils; corrugated iron sheets; roofing tiles
Suburbans with small gardens and groves; sport grounds; industrial used areas; intensively used agricultural fields;
abandoned agricultural land
Public parks; small plots of ruderal plant communities
Open evergreen to semi-deciduous broad-leaved forests fragments; forest-bush transitions; plantations; water
courses
Cloud forests fragments; dense evergreen to semi-deciduous broad-leaved forests fragments; water courses
root mean square equation (RMSE) (Eq. (1)), resulting in a RMSE of
10.18 m.
RMSE =
Fig. 1. Distribution of sample sites (triangles) within the study area (polygon).
Additionally, the extremely steep flanks of the Río Chama and
Albarregas valleys were not included in the survey.
Each plot was 50 m2 in size (10 m × 5 m) and its geographic position and elevation were measured with a handhold GPS receiver
(etrex Summit, Garmin, USA). Representative botanical specimens
were collected for each species and deposited at the herbarium
of the Universidad de Los Andes, Mérida, Venezuela (MERC). Epiphytes of the upper tree strata were collected using telescope
pruning scissors or identified by means of binoculars. Species
identification relied predominantly on Davidse, Sousa, and Chater
(1994), Hornung (1998), Smith (1971), and Smith and Downs
(1977), or on comparison with well-determined herbarium specimens of the herbarium MERC.
2.3. Remote sensing data and urban habitat classification
An Advanced Spaceborne Thermal Emission and Reflection
Radiometer (ASTER) satellite image consisting of a L1A ASTER scene
was used to classify the urban area of Mérida. It was collected by the
ASTER/Terra sensor on February 1, 2004 and only 1% cloud cover
was present at the time. The spatial resolution of the ASTER image
differs between the three spectral groups of VNIR, SWIR and TIR. In
this study we considered the first nine bands of the image, the VNIR
spectral region (bands 1–3), which is characterized by a spatial resolution of 15 m, and the SWIR (bands 4–9) wavelength region with
a spatial resolution of 30 m. The spectral region TIR with a spatial
resolution of 90 m was not included. The image was obtained in
a HDF EOS format with image center coordinates of 71◦ 11′ 06′′ W
and 8◦ 39′ 49′′ N. Georeferencing was carried out with the image
processing software TNT mips 6.5 (Microimages, Lincoln, USA) by
using an affine georeferencing model. Therefore, a total of 7 Ground
Control Points (GCP) were collected with the help of a handhold GPS
receiver. We assessed the relative vertical spatial accuracy with the
n
d2
i=1 i
n
(1)
di2 = Zest − Zobs · Zest is the DEM value, Zobs the field-measured
elevation value, n the number of collected GCPs.
We performed a supervised maximum likelihood classification
of the study region, using a soft classifier (De Smith, Goodchild,
& Longley, 2009). The classification refers to 85 training sites
based on field survey. The vegetation-impervious surface-soil (VI-S) model was taken into consideration to develop the training
site assortment, as is recommended during classification of urban
environments. The basic idea of the V-I-S model is to simplify the
heterogeneous urban area and divide it into three main components: vegetation, impervious surface, and soil (Hung, 2002). Due to
the fact that homogenous training sites generally improve the land
cover classification, our training sites were homogenous whenever
possible, leading to 19 land cover classes. The gradual transition
between land use and land cover within urban areas has led to the
consolidation of the two under the heading land cover.
The qualitative evaluation of the land cover classification’s performance was carried out by a visual assessment of an aerial
photograph obtained by the mission ISS005 of the International
Space Station in October 2002 and an up-to-date roadmap. Additionally, GCPs were taken during two field excursions in May and
two in September 2007.
The 19 thematic land cover classes were grouped into five major
categories (zones) based on the percentage of soil sealing using the
software ArcGIS 10.0 (ESRI, Redlands, USA) (Table 1). Soil sealing is
defined as soils that have been made impervious to water by human
construction activities. The highest degree of soil sealing is found in
the core area of the city where asphalted streets, buildings and further highly impervious compacted soils predominate. The degree
of soil sealing is strongly linked to the observed land cover, and
thus reflects the potential occurrence of trees that provide the main
substrate for epiphytic bromeliads. Furthermore, the resolution of
our satellite image did not allow for a clear differentiation between
the vegetation-covered riverbanks and the water bodies during the
process of supervised classification. For this reason water bodies
were not classified and riverbanks were partly assigned to zones 4
and 5 considering the respective vegetation.
To evaluate the quality of the supervised classification results
of the five major zones a quantitative accuracy assessment was
conducted in GRASS GIS, version 6.4.0 (GRASS Development Team,
2010). Two hundred random control points were allocated on
the aerial photograph of 2002. Each control point was assigned a
reference value. The reference values were compared to the classification value of the respective pixel. Producer’s, user’s, overall
accuracy, and the kappa coefficient (see Congalton, 1991; Foody,
2002) were calculated in Microsoft Excel (2007).
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C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
2.4. Habitat suitability modelling (HSM)
In this study, we follow the terminology of Bradley et al. (2012)
and use the term HSM to describe models of potential species
distribution based on environmental correlates. Predictive models of a species’ habitat were created using Maxent 3.3.3 (Phillips,
Anderson, & Schapire, 2006; Phillips, Dudík, & Schapire, 2004),
which has proven powerful for this purpose (Buermann et al., 2008;
Elith et al., 2011; Lentz, Bye, & Sánchez-Cordero, 2008; PratesClark, Saatchi, & Agosti, 2008). Maxent utilizes presence-only point
occurrences with high performance even on small datasets (Elith
et al., 2006; Evangelista et al., 2008; Loiselle et al., 2008; Pearson,
Raxworthy, Nakamura, & Peterson, 2007; Phillips et al., 2004; Wisz
et al., 2008). As predictor variables we used the VNIR and the SWIR
range of the ASTER image. Furthermore, we included a DEM taken
by the Shuttle Radar Topography Mission (SRTM) with a resolution
of 90 m. The DEM was obtained from the U.S. Geological Survey
(USGS) and preprocessed using spline interpolation and a low-pass
filter in GRASS GIS, version 6.4.0 (GRASS Development Team, 2010)
to remove gaps and random errors (Li, Zhu, & Gold, 2005; Neteler
& Mitasova, 2002). Thereafter, the DEM and the bands 1–3 of the
ASTER image were resampled to 30 m resolution to obtain an equal
spatial accuracy of the layers. The derivates slope and aspect were
calculated using the DEM in ArcGIS 9.2 (ESRI, Redlands, USA).
The number of point occurrences is a limiting factor for HSMs.
Studies by Hernandez, Graham, Master, and Albert (2006), Pearson
et al. (2007), and Wisz et al. (2008) unequivocally found that
Maxent can still build meaningful models at a minimum of 5–10
occurrences. Therefore, we choose the mean of this range as a
critical value and included only species with a minimum of eight
occurrences in the analysis, thus excluding Guzmania mitis, Tillandsia longifolia, Tillandsia pruinosa, Tillandsia schiedeana, and Tillandsia
schultzei. Species occurrence data usually are split into training and
test data to provide statistical analyses of the HSMs. The available
data set for the present study was limited in size. Consequently,
training and test data sets would have become too small by splitting for an appropriate statistic testing (Pearson et al., 2007). As
recommended by Phillips (2006), when working with small data
sets, we ran our models with an 8-fold cross-validation and a testpercentage of 10% during each run. We evaluated the accuracy of
the models, considering the average of the Test-AUC value (area
under the curve) calculated for each single species, a commonly
used but still controversial measure (Lobo, Jiménez-Valverde, &
Real, 2008). We therefore tested the significance of the obtained
AUC values of the species’ habitat suitability models using the nullmodel approach described in Raes and ter Steege (2007). To build
the null distribution we ran 1000 random models with randomly
drawn sample localities equal to the number of observations for
each species and the same environmental predictors as described
in the Maxent procedure. We used a 95% confidence interval to test
if the HSM performs significantly better than expected by chance.
For the further statistic analyses, bromeliad species were classified either as CAM or C3 species according to data from Martin
(1994) and Crayn, Winter, and Smith (2004). Species were also classified according to their ability to impound water with their densely
arranged rosette leaves, thus, species with tank habit were compared to species without or with a weakly developed tank habit.
Our classification is based on morphological observations.
Pearson correlations and a two-tailed t-test were used to test
for trends of the point occurrence probabilities for each species
and for CAM versus C3 species across urban soil sealing zones.
For calculating the correlation coefficients we used 10,000 point
occurrence probabilities randomly sampled from the total probability distribution per zone and species. Additionally, differences
between mean occurrence probabilities (of the total point occurrence probabilities) per zone of CAM versus C3 species were tested
using a two-tailed t-test. All statistical tests were run in R, version
2.15.1 (R Core Team, 2012).
3. Results
3.1. Identification, evaluation and spatial distribution of urban
zones based on land cover classes
The supervised satellite image classification of Mérida city
resulted in a thematic map of 19 land cover classes. Grouping of
these classes into five major urban zones based on soil sealing
shows that the first two zones (50–100% sealed soils) make up
∼60% of the total urban area (Table 1 and Fig. 2). These highly sealed
surfaces include the core area of Mérida (ca. 12%), housing developments with small gardens and groves, areas of intensive agricultural
or industrial use, and abandoned agricultural land. Approximately
6% are covered by urban spaces, as well as small areas of ruderal
plant communities, both being categorized as Zone 3. A total of
about 10% are watercourses which correspond to zones 4 and 5.
Zone 4 is characterized by relatively low soil-sealing (5–24.9%). It is
covered by open evergreen to semi-deciduous broad-leaved forest
fragments, plantations, and forest-bush transitions. About 19% of
the total area is covered by closely forested areas, of which around
4% are cloud forest fragments (Zone 5). The accuracy assessment
of the classification results of the five major urban zones in Mérida
city is summarized in Table 2. The overall classification accuracy is
74.11% and the kappa coefficient is 0.45.
2.5. Modelled species richness and statistical analyses
Our species richness maps were obtained by aggregating the
HSMs of the single species for which the Test-AUC value of the HSM
significantly differed from random, excluding the three species
Tillandsia balbisiana, Tillandsia biflora, and Tillandsia myriantha.
A Visual Basic routine (described in Schmidt, 2006) counted for
each grid cell species with a probability of occurrence above the
‘maximum training sensitivity plus specificity threshold’ as recommended by Liu, Berry, Dawson, and Pearson (2005). In order to
evaluate the similarity between the HSMs, a simple Pearson correlation analysis was carried out (Table 4). For the calculation of the
correlation coefficients we used each pixel-value of the HSMs.
Fig. 2. Map of land cover classes within Mérida city based on the supervised satellite
image classification.
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
111
Table 2
Accuracy assessment of the five major urban zones of Mérida city.
Classification data
Data of geo-referenced aerial photograph
Zone 1
Zone 2
Zone 4
Zone 5
Zone 1
Zone 2
Zone 3
Zone 4
Zone 5
23
1
6
2
0
5
46
0
1
3
3
2
6
3
1
2
9
0
32
3
0
4
0
6
39
33
62
12
44
46
Column total
32
55
15
46
49
197
User’s accuracy (%)
Producer’s accuracy (%)
69.7
71.8
74.2
83.6
50
40
72.7
69.6
84.8
79.6
Overall accuracy (%)
Kappa coefficient (k)
Chance agreement
Zone 3
Row total
69.7
74.1
0.45
0.23
3.2. Bromeliad diversity and species occurrences
A total of 20 bromeliad species were recorded in the study area
(Table 3), all belonging to the subfamily Tillandsioideae, and usually growing epiphytic (occasionally also saxicolous or terrestrial).
Tillandsia (14 species) was the most diverse genus, followed by Racinaea (3), Guzmania (2), and Catopsis (1). Of these, eleven species are
C3 plants, eight are CAM plants, and for one species (T. myriantha)
data is ambiguous. Ten species exhibit a tank habit (impounding
water), four possess a poorly developed tank habit, while six species
are classified as lacking a tank habit (Table 3).
The most frequent species was Tillandsia recurvata, which was
found in 57 plots, whereas T. pruinosa was recorded in only two
plots. Species richness was higher at elevations above 1400 m,
with a maximum of 12 species per plot at Loma de la Virgen
site (1869 m), a grazing area with many shade trees. Four plots
contained only a single species (T. recurvata).
The most widespread species are Catopsis nutans, Guzmania monostachia, Racinaea tenuispica, Tillandsia fendleri, Tillandsia
juncea, T. recurvata, Tillandsia usneoides, and Tillandsia variabilis,
occurring in all five urban zones. Racinaea spiculosa, T. biflora,
Tillandsia complanata, T. myriantha, and T. schiedeana were reported
from zones 2 through 5. The other species show an unequal
distribution, especially G. mitis, which is confined to the two leastsealed urban zones. G. mitis, Racinaea tetrantha, T. balbisiana, T.
longifolia, T. myriantha, T. pruinosa, T. schiedeana, and T. schultzei
were comparatively rare with less than ten point occurrences.
C. nutans was recorded above 1200 m and mostly in the urban
center, less frequently in the semi-natural areas, and was absent
from the northern cloud forest area. G. monostachia was recorded
in areas above 1300 m and was widespread in central and marginal
areas. It was especially frequent in gardens and public parks. R.
tenuispica was among the most widespread species of the city,
occurring in the center, urban pastureland, and forests. It was only
absent from the north-western cloud forest and some highly sealed
areas. T. usneoides and T. variabilis showed a similar distribution and
were reported from areas above 1200 m from pastureland, parks,
and highly sealed areas, but not from the north-western cloud forest. T. recurvata was observed most frequently in the highly sealed
areas and was less frequent in pastureland and forest areas at the
periphery. It was absent from the north-western cloud forest. T.
balbisiana was a rare species that occurred only below 1600 m in
green areas and parks, partially also in highly sealed areas. Tillandsia fasciculata was documented in semi-natural and highly sealed
Table 3
List of Bromeliaceae found in the study site and their ecological and ecophysiological characteristics. Distribution and elevation according to Smith and Downs (1977).
Photosynthetic pathway according to Martin (1994)a or Crayn et al. (2004)b . Tank habit refers to the rosulate, basally tight leaves that allow the plants to accumulate water
and create phytotelmata. Some species (marked by parentheses) have more or less loosely arranged or narrow leaves and may impound only small volumes of water. Species
names according to Luther (2010).
Species
Distribution
Elevation range
(m a.s.l.)
Photosynthetic
pathway
Tank habit
Catopsis nutans (Sw.) Griseb.
Guzmania mitis L.B. Sm.
Guzmania monostachia (L.) Rusby ex Mez in A. DC. & C. DC.
Racinaea spiculosa (Griseb.) M.A.Spencer & L.B.Sm.
Racinaea tenuispica (André) M.A.Spencer & L.B.Sm.
Racinaea tetrantha (Ruiz & Pav.) M.A. Spencer & L.B. Sm.
Tillandsia balbisiana Schult. f., in Roem. & Schult.
Tillandsia biflora Ruiz & Pav.
Tillandsia complanata Benth.
Tillandsia fasciculata Sw.
Tillandsia fendleri Griseb.
Tillandsia juncea (Ruiz & Pav.) Poir.
Tillandsia longifolia Baker
Tillandsia myriantha Baker
Tillandsia pruinosa Sw.
Tillandsia recurvata (L.) L.
Tillandsia schiedeana Steud.
Tillandsia schultzei Harms
Tillandsia usneoides (L.) L.
Tillandsia variabilis Schltdl.
Mexico to Ecuador
Costa Rica to Ecuador
USA to Bolivia and Brazil
Costa Rica to Bolivia and Brazil
Venezuela and Greater Antilles to Peru
Venezuela to Bolivia
USA to Colombia
Costa Rica to Bolivia
Costa Rica to Bolivia
USA to Colombia
Venezuela and Greater Antilles to Bolivia
USA to Bolivia
Costa Rica to Peru
Venezuela and Colombia
Mexico to Ecuador and Brazil
USA to Argentina
Mexico to Colombia and Venezuela
Venezuela and Colombia
USA to Chile
Mexico to Venezuela
0–1700
1600–3300
900–1500
300–2800
300–2100
750–3300
30–1500
1300–3000
800–3500
50–1600
400–2900
150–1900
750–2800
1300–2200
0–1300
0–3000
50–1800
1200–2800
30–2400
100–2200
C3 ab
C3 ab
C3 -[CAM]a C3 b
C3 ab
C3 ab
C3 ab
CAMab
[CAMa ] C3 b
C3 ab
CAMab
C3 ab
CAMab
C3 ab
CAMa C3 b
CAMb
CAMab
CAMab
C3 b
CAMa
CAMb
Yes
Yes
Yes
Yes
Yes
Yes
No
Yes
Yes
(Yes)
Yes
No
(Yes)
(Yes)
No
No
No
Yes
No
(Yes)
112
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
Fig. 3. (a) Occurrences (dots) and modelled distributions of Bromeliaceae species in the city of Mérida (polygon). (b) Modelled species diversity.
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
1
1
0.97
1
0.93
0.90
T. recurvata
T. usneoides
T. variabilis
areas below 1600 m. T. juncea was found above 1200 m and was
widespread across a variety of urban habitats ranging from green
areas, parks and pastureland to forests. T. fendleri was recorded at
areas above 1500 m and occurred especially in green areas, parks,
pastureland and forests. T. biflora grew above 1750 m in forests and
pastureland, but was absent from the central urban area. A similar distribution was observed for T. complanata. T. longifolia was a
rare species occurring only in the north-western cloud forest above
2100 m. R. spiculosa occurred above 1700 m in forests, pastureland
and cropland, but was absent from highly sealed areas of the city
center. T. myriantha was observed above 1700 m in pastureland,
gardens and groves.
113
1
0.85
0.94
0.93
1
0.58
0.45
0.59
0.64
1
0
0.62
0.77
0.66
0.60
1
−0.06
0.49
0.16
−0.02
0.08
0.12
1
0.88
−0.04
0.36
0.11
−0.05
0.02
0.06
1
0.01
0.07
0.59
0.64
0.92
0.92
0.97
0.97
1
0.11
0.73
0.93
0.01
0.47
0.22
0.01
0.14
0.16
1
0.14
0.87
0.08
0.12
0.53
0.59
0.82
0.80
0.87
0.92
T. fendleri
T. fasciculata
T. complanata
R. tetrantha
R. tenuispica
R. spiculosa
G. monostachia
C. nutans
1
0.84
0.06
0.97
−0.02
0.03
0.61
0.63
0.90
0.94
0.97
0.96
C. nutans
G. monostachia
R. spiculosa
R. tenuispica
R. tetrantha
T. complanata
T. fasciculata
T. fendleri
T. juncea
T. recurvata
T. usneoides
T. variabilis
Table 4
Values of the Pearson correlation coefficients of the modelled habitat suitability maps.
Species HSMs were generated for 15 species, with 12 of the modelled distribution patterns differing significantly from a random
one (Appendix A).
C. nutans, G. monostachia, R. tenuispica, T. juncea, T. recurvata, T.
usneoides, and T. variabilis show similar distribution ranges according to the HSMs (Fig. 3a and Table 4), each species prevailing in
the city center and, thus, in the area of maximum anthropogenic
modification of the landscape. A contrasting pattern is observed
in R. spiculosa, R. tetrantha, and T. complanata, which show higher
occurrence probabilities in areas along the two rivers and outside
the urban sector. It is also remarkable that the percental contribution of the environmental variable slope is relatively high (40.3%,
50.4%, and 49.3%) in these models. Thus, they predominantly occur
in shaded, forested depressions along the western mountainside
(>50% occurrence probability). However, R. tetrantha shows generally the lowest probability to occur whereas T. myriantha shows the
highest.
T. fendleri was predicted to be absent from the southern part
of Mérida, while the north-eastern part of Mérida’s center shows
the highest cumulative probability (>60%). Also the program Maxent considered the contribution of the variables DEM (25%) and
slope (42.6%) relatively high in this case. In contrast, T. fasciculata
has the highest predicted distribution for the south-western part
of the study area (>60% probability). The percent contribution of
the environmental variable DEM to the model of T. fasciculata was
highest (59%).
According to the modelled habitat suitability, the species show
different probabilities for their occurrence in the five urban zones
(Fig. 4). There is a highly significant trend (p < 0.001) to occur in
areas with higher soil sealing for C. nutans (r = 0.25, t = 58.3), G.
monostachia (r = 0.13, t = 29.5), R. tenuispica (r = 0.13, t = 30.3), T. fasciculata (r = 0.08, t = 17.6), T. fendleri (r = 0.04, t = 9.9), T. recurvata
(r = 0.25, t = 58.9), T. usneoides (r = 0.11, t = 23.8), and T. variabilis
(r = 0.12, t = 27.3). An inverse trend significant at p < 0.001 is
observed for R. spiculosa (r = −0.38, t = −91.5), R. tetrantha (r = −0.29,
t = −67.9), and T. complanata (r = −0.35, t = −85.0). The distributions
of CAM versus C3 species were different (Fig. 5), but a trend toward
higher occurrence probabilities in zones with higher soil sealing is
only significant for CAM species (r = 0.47, t = 2.582, df = 23, p < 0.017;
for C3 species: r = −0.064, t = −0.3671, df = 33, p = 0.716). Because
the species with a well-developed tank habit correspond exactly
with those with a C3 physiology, they do not show any significant
trend across the land cover zones. In contrast, the non- or poorly
impounding species have higher occurrence probabilities in zones
with higher soil sealing.
Our modelled map of species richness predicts the highest
species diversity in the core area of the city. A relatively high probability of species diversity can be also observed along the two
watercourses, the Río Chama and Río Albarregas. The lowest species
diversity is displayed in the more natural to semi-natural habitats.
T. juncea
3.3. Modelled habitat suitability and species richness
114
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
Fig. 4. Boxplots of point occurrence probabilities per urban zone (means of the percentage of soil sealing) for each species. Only species occurring ≥8 times per study plot
were considered. Analysis based on 10,000 randomly sampled probabilities per zone.
Fig. 5. Scatterplots of mean occurrence probabilities for each species per urban zone (means of the percentage of soil sealing). (left) CAM species and (right) C3 species.
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
Among the latter, the highest diversity has been modelled for the
humid mountain depressions.
4. Discussion and conclusions
4.1. Urban diversity of Bromeliaceae and the role of CAM versus
C3 species
CAM plants as compared to C3 plants are generally more
drought-tolerant due to their peculiar physiology. Drought
tolerance, in turn, is favourable for successfully colonizing the generally drier urban habitats. Therefore, it is not surprising that the
CAM species among the bromeliads investigated here show higher
occurrence probabilities in urban zones with high soil sealing.
Comparing our data with two floristic inventories of successional and mature upper montane rainforests between 2300 and
3300 m a.s.l. in the immediate vicinity of Mérida city (La Montaña
site, 1.5 ha, Kelly et al., 1994; La Caña site, ∼1.2 ha, Schneider, 2001)
reveals that all their species lacking in our study area but known to
occur also at altitudes covered by Mérida city are C3 plants (Mezobromelia capituligera [=Tillandsia capituligera], Tillandsia compacta,
Tillandsia denudata, Tillandsia tovarensis, Vriesea robusta, Vriesea
tequendamae, Werauhia cowellii [=Vriesea cowellii]). Thus, CAM bromeliads are not only well-adapted to live in tropical urban habitats,
but are also suitable indicators for the degree of urbanization.
The absence of the C3 species of the La Montaña and La Caña
sites mentioned above from our study area may have various
reasons. They might have been unable to migrate into the city,
gone extinct therein, or the number of study plots may have
been insufficient to discover all bromeliad species actually present.
Especially critical for the successful colonization of isolated urban
phorophytes by epiphytes is the distance that the diaspores have
to travel from the source populations. Although the bromeliads
observed in this study all belong to the pogonochorous (plumed,
wind-dispersed) subfamily Tillandsioideae, isolation by distance is
certainly an important reason for a species-poor epiphytic flora
(Hietz-Seifert, Hietz, & Guevara, 1996; Wolf, 2005). Local extinction may also play a critical role as it has been well-established that
already after a decade of isolation the epiphytic flora of phorophytes
(i.e., the plants carrying the epiphytes) substantially impoverishes
regarding species richness, mainly due to the altered microclimatic conditions on isolated trees (Nöske et al., 2008; Werner &
Gradstein, 2008; Werner, Homeier, & Gradstein, 2005). As isolation of phorophytes or alternative substrates and the therewith
associated altered microclimate is a longstanding condition in
most of the urban habitats, these factors are supposed to be the
main triggers of species decline. On the other hand, the city’s
flora is still comparatively rich, considering that it contains 36%
of the total bromeliad diversity of the state of Mérida (56 spp., see
Hornung, 1998; Hornung & Gaviria, 1999) which covers an area
of 11,300 km2 . These numbers illustrate the resilience of many
bromeliad species to the ecological changes caused by urbanization. All bromeliad species encountered are epiphytes, which in
turn depend on their phorophytes. Although the microclimate differs between the urban and natural non-urban sites, the epiphytic
substrate is similar throughout. The tiny T. recurvata is probably
the only species with the ability to colonize new habitats in urban
areas, since it often grows on telephone wires or similar substrates.
Therefore, resilience is also due to competitive advantage in the
epiphytic niche over other urban angiosperm species.
The relatively high modelled species diversity along the watercourses (Fig. 3b) may be due to the fact that these areas are mainly
covered by old phorophytes, are relatively humid, and are less
influenced by human impact. To explain the relatively high diversity of bromeliads in the core area of Mérida city two factors are
115
important. First, the upper montane rainforests above 2300 m in
the vicinity of Mérida do not harbour any CAM species (Kelly et al.,
1994; Schneider, 2001), which means that this species group apparently has a lower potential for colonizing the more natural areas
in the marginal sectors of the city. Second, the C3 species colonize successfully the natural areas, but also occur in the core areas
with higher soil sealing. Thus, the core area is habitat to both
groups, whereas the marginal sectors are less favourable for CAM
species.
4.2. The utility of remote sensing data for habitat suitability
modelling in urban areas
Generally our HSMs were in line with field experience, and high
AUC values indicate a good model fit. Only for three species with
comparatively few (T. balbisiana, T. biflora) or clustered (T. myriantha) occurrence points, test AUCs did not significantly differ from
those of the null-models.
Previous studies showed that plant distributions in cities are
strongly influenced by human impact and that each component
of the urban environment, that is, the different types of built-up
areas, has its own specific set of species (Godefroid & Koedam, 2007;
McKinney, 2006). Such a pattern was also confirmed by our data on
bromeliads with C3 and CAM species showing different success in
colonizing the urban zones.
The resolution of environmental variables is of particular
importance for HSMs. Especially in heterogeneous fragmented
landscapes, species distributions cannot be reflected by coarse scale
environmental data like interpolated temperature or precipitation
maps (König, Schmidt, & Müller, 2009). In contrast, high resolution satellite images can reflect the heterogeneity of surfaces on a
very fine scale, resulting in an excellent environmental predictor in
urban environmental studies. Several studies (e.g. Buermann et al.,
2008; Cord & Rödder, 2011; Zimmermann et al., 2007) have already
shown the predictive power of remote sensing data when incorporated into HSM approaches. Cord and Rödder (2011) found that for
most species HSMs on the basis of remote sensing data combined
with climate data yield the best results. However, the resolution
of interpolated climate data for Mérida city is not high enough to
be applicable for our study. Additionally, inferences concerning the
improvement in model success for remote sensing data are limited
by the relatively large contribution of the elevation and the slope
to most of the HSMs. One major drawback concerning the applicability of remote sensing data in urban areas is the phenomenon
of mixed pixels (Wang, 1990). The urban ground heterogeneity
results in pixels that correspond to more than one land cover type
and it is thus difficult to assign them unambiguously. Nonetheless, in our study the use of a maximum likelihood classification
with a soft classifier in combination with a homogenous selection
of training sites led to a satisfying result regarding the scope of our
investigation.
The accuracy assessment of the supervised classification of the
five major urban zones shows a fair overall accuracy of 74.1%
(Congalton, 1991; Table 2). Misclassification results from the complex spectral signatures of urban landscapes with mixed pixels and
the small fractions of zone types within the city. However, when
comparing k and the chance agreement the classification accuracy
is 45% better than it would have been expected only by chance. In
general the calculated producer’s and user’s accuracies are sufficiently high to distinguish between the five urban zones (Table 2).
Only Zone 3 has a relatively low producer’s and user’s accuracy. This
can be explained by the high fragmentation of this zone, which is
composed of public parks and small plots of ruderal plant communities (Table 1). It is the smallest zone of all and covers only
6% of the study area. High fragmentation of urban environments
often results in misclassified pixel-values, as a consequence of the
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
116
insufficient image resolution and the combination of the urban
landscapes element size in relation to the sensor cell size. This leads
to mixed pixels, which are a well-known phenomenon in urban
landscapes (Lillesand & Kiefer, 2008; Lu & Weng, 2004).
The classification accuracy can be improved by using higher resolution remote sensing data and advanced classification technics
(object oriented classification). This, however, is beyond the scope
of this study.
4.3. Conclusions
The uninterrupted trend of rural-to-urban migration in tropical countries will result in a higher pressure on urban biodiversity,
rendering effective conservation strategies for urban species of vital
importance. Here we have shown that the incorporation of remote
sensing data into habitat suitability modelling is a powerful, costeffective method to visualize fine-scale biodiversity patterns in
complex tropical urban habitats. Understanding the potential distribution of the species, in turn, is essential for identifying more
precisely the specific needs for maintaining diversity in urban
areas, thus enhancing conservation planning. Bromeliaceae is a
plant group resilient to urbanization due to their multiple morphological and physiological adaptations. It is thus a group suitable
to work with for studies of urban environments related to biodiversity patterns. Especially the relative contribution of C3 versus
CAM species to the total richness of bromeliad species may prove
a valuable indicator, with the extreme predominance of the latter indicating not only a trend toward aridification and increased
soil sealing of the local landscape but also a potential loss of the
total diversity (due to the joint loss of more mesic species). However, this needs to be tested more thoroughly in future studies.
Since bromeliads provide secondary aquatic habitats for insects or
amphibians in the water-impounding tank species (phytotelmata),
they contribute to the overall urban biodiversity. On the other hand,
they participate in the spreading of insect-borne epidemic diseases
such as dengue fever (Frank, 1983; Lounibos, O’Meara, Nishimura,
& Escher, 2003). Thus, a better knowledge of their potential distribution in urban areas will be helpful to monitor and control such
diseases.
Acknowledgements
We like to thank M. Alberto, L. Anzola for help during fieldwork in Venezuela, K. König and G. Bocksberger for helpful advices
regarding the modelling approach and statistical analyses, S. Connery and R. Byer for language advices, and three anonymous
reviewers for fruitful comments on an earlier version of the
manuscript. The first author is also grateful to the German Academic Exchange Service (DAAD) for financial support. We also
acknowledge funding by the Biodiversity and Climate Research
Center (BiK-F), Frankfurt.
Appendix A.
Test-AUC values of the HSMs and the null model. Species for
which the Test-AUC value of the HSM does not differ significantly
from random are highlighted by an asterisk. Additionally, the percent contributions of the environmental variables to the Maxent
models are list, when they a higher than 10%.
Species
Number of species
occurrences
Average of the
test AUC
AUC of the
null-model
Band 2
Catopsis nutans
Gutzmania monostachia
Racinaea spiculosa
Racinaea tenuispica
Racinaea tetrantha
Tillandsia balbisiana
Tillandsia biflora
Tillandsia complanata
Tillandsia fasciculata
Tillandsia fendleri
Tillandsia juncea
Tillandsia myriantha
Tillandsia recurvata
Tillandsia usneoides
Tillandsia variabilis
46
24
14
55
11
8
15
11
17
40
34
8
57
54
50
0.83
0.87
0.79
0.82
0.95
0.77*
0.8*
0.87
0.92
0.83
0.84
0.70*
0.82
0.81
0.85
0.74
0.8
0.77
0.73
0.79
0.80
0.85
0.79
0.83
0.76
0.77
0.80
0.72
0.73
0.73
–
–
32.5
–
20.9
–
13.4
17.8
14.4
–
14.9
21.6
–
–
10
Band 3
–
–
14.4
–
–
–
–
–
–
–
–
11.3
–
–
–
Band 5
38.8
12.7
–
33.7
–
–
–
–
–
14.9
26
–
29.6
35
26.9
Band 6
–
–
–
–
–
22
–
–
–
–
–
–
–
–
–
DEM
Slope
–
27.1
–
12.6
21.2
54
16
23
59
25.6
–
–
14
11.5
11.3
33.7
39.2
40.3
30.1
50.4
11.7
60
49.3
15.7
42.6
38.8
57.1
38.6
33.4
39.9
C. Judith et al. / Landscape and Urban Planning 120 (2013) 107–118
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