See

discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/301732403

Complementary Ecological Approaches to

Understand Decreases in Frog Diversity in
Altered Andean Ecosystems
Article in South American Journal of Herpetology April 2016
DOI: 10.2994/SAJH-D-15-00015.1

CITATIONS

READS

50

2 authors:
Javier Mendez Narvaez

Wilmar Bolivar

Boston University

Universidad del Valle (Colombia)

14 PUBLICATIONS 17 CITATIONS

34 PUBLICATIONS 424 CITATIONS

SEE PROFILE

SEE PROFILE

All content following this page was uploaded by Javier Mendez Narvaez on 03 May 2016.

The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document
and are linked to publications on ResearchGate, letting you access and read them immediately.

Complementary Ecological Approaches to Understand Decreases in Frog

Diversity in Altered Andean Ecosystems
Author(s): Javier Mndez-Narvez , Wilmar Bolvar-G
Source: South American Journal of Herpetology, 11(1):1-11.
Published By: Brazilian Society of Herpetology
DOI: http://dx.doi.org/10.2994/SAJH-D-15-00015.1
URL: http://www.bioone.org/doi/full/10.2994/SAJH-D-15-00015.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological,
and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books
published by nonprofit societies, associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of
BioOnes Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial
inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions,
research libraries, and research funders in the common goal of maximizing access to critical research.

South American Journal of Herpetology, 11(1), 2016, 111

2016 Brazilian Society of Herpetology

Complementary Ecological Approaches to Understand

Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez1,2,*, Wilmar BolvarG1,3


3
*
1
2

Calima, Fundacin para la Investigacin de la Biodiversidad y Conservacin en el Trpico. Carrera 67A # 33b16, Cali, Colombia.
Biology department, Boston University, 5 Cummington Mall, Boston, MA 02215, USA.
Biology Department, Grupo de Investigacin en Ecologa Animal, Universidad del Valle. A.A. 25360, Cali, Colombia.
Corresponding author. Email: javier0620@gmail.com

Abstract. The Andes Mountains of South America are considered one of the most biologically diverse and threatened areas in the world.
Habitat destruction in this area is among the most common causes of amphibian population declines and extinction, but few studies have
used complementary approaches to understand the interplay between habitat transformation and microhabitat use by amphibians. We
studied the anuran diversity in modified vegetation cover types in a cloud forest in the tropical Andes of Colombia in order to compare components of biological diversity and microhabitat preferences among forested and human-altered habitats. Secondary Forest and Riparian
Forest were the vegetation cover type with the highest local diversity, whereas the highest turnover was between the forested and humanaltered areas. The species in the assemblage showed specific microhabitat associations with the substrate and the vertical stratification, with
lower mean values of niche overlap between species pairs in forested area than in human altered areas. These results show how anthropic
intervention creates less favorable vegetation cover types for some species of anurans and the way in which preferences for a specific microhabitat could influence distribution in these vegetation cover type.
Keywords. Anthropic intervention; Anurans; Niche preferences; Species reduction.
Resumen. La Cordillera de los Andes en Amrica se considera una de las reas de mayor diversidad biolgica y ms amenazadas en el mundo.
La destruccin del hbitat en esta regin figura entre las causas ms comunes de declive poblacional y extincin en poblaciones anfibios. Sin
embargo, pocos estudios han usado aproximaciones complementarias para entender la interaccin entre la transformacin del hbitat y el
uso de microhbitat en anfibios. Nosotros estudiamos la diversidad de anuros en diferentes tipos de cobertura vegetal modificadas, en un
bosque de niebla en los Andes Tropicales de Colombia, con el fin de comparar diferentes componentes de la diversidad biolgica y seleccin
de microhbitat entre reas boscosas y con modificacin antropognica. El Bosque Secundario y el Bosque Ripario fueron el tipo de cobertura
vegetal con la mayor diversidad local de especies, mientras el mayor recambio fue entre reas boscosas y alteradas por el hombre. Las especies
en el ensamble mostraron asociaciones especificas con el sustrato y en su estratificacin vertical, con valores promedio de solapamiento de
nicho mas bajos entre pares de especies en reas boscosas comparadas con modificacin antropognica. Estos resultados evidencian como la
intervencin antropognica crea cobertura de bosques menos favorables para algunas especies de anuros y la forma en que las preferencias
de stos por un microhbitat especifico pueden influir en su distribucin en estas coberturas de vegetacin.

INTRODUCTION
Population declines and extinction of amphibian
species have been the center of extensive debate and research in the last decade (Stuart etal., 2004; 2008). Direct
and indirect impacts of human activities are considered
the main cause of this worldwide phenomenon (Alford
and Richards, 1999; Collins and Storfer, 2003; Pounds
etal., 2006). This effect is not geographically random and
has affected mainly Neotropical amphibian species (Stuart
etal., 2004). In Latin America, although some studies that
show the population declines in a geographic and taxonomic context, most have highlighted the negative impact
on particular amphibian families that inhabit high Andean ecosystems (Lips etal., 2005a,b; La Marca etal., 2005).
The high humidity, abundant water sources, and
geographic barriers in Andean ecosystems have favored
historically the presence and diversification of amphibians (Navas, 2003; 2006; Guarnizo etal., 2015), resulting
in the greatest diversity of amphibian species per area in
Submitted: 16 July 2015
Accepted: 04 March 2016

the world (Myers et al., 2000; Young et al., 2004; Hutter et al., 2013). In particular, Colombia attains one of
the most diverse anuran fauna in the world with ca.714
species (Lynch, 1998; Acosta-Galvis, 2000; Kattan etal.,
2004) and there are probably many more cryptic species
to describe (Kieswetter and Schneider, 2013; Guarnizo
etal., 2015). However, it also has the highest number of
threatened amphibian species (Angulo etal., 2006). The
most susceptible species are those distributed in Andean
forested habitats and Amazonian habitats, where both
the strongest processes of habitat destruction (Kattan
and lvarez, 1996; Cabrera etal., 2011; Rueda-Almonacid
etal., 2004) and the highest species richness (Lynch etal.,
1997; Kattan etal., 2004) have been reported. Additional
causes such as emergent pathogens and global climate
change (Pounds et al., 2006; Alford et al., 2007, Foden
etal. 2013) have also been considered to explain amphibian decline, but we are unaware of any studies that have
considered ecological aspects like niche differences and
components of biological diversity to explain it.

Handling Editor: Ralph A. Saporito

doi: 10.2994/SAJHD1500015.1

South American Journal of Herpetology, 11(1), 2016, 111

In order to study species assemblages, two approaches have been most commonly used: components of
biological diversity and ecological species niche. The first
has been used to understand the effect of habitat change
on assemblages (Whittaker, 1972; Moreno, 2001; Pineda
and Halffter, 2005; Pineda et al., 2005). Alpha diversity
(local diversity) is one of the most commonly used estimates, but it has been suggested that the study of beta
diversity (species turnover) across vegetation cover types
or localities allows a better understanding to determine
which factors define species assemblages: distance, environmental heterogeneity, or historical processes (Condit
et al., 2002; Halffter and Moreno, 2005). Species niche
partitioning has been used to understand how species diversity and composition change along environmental or
spatiotemporal gradients (Chase and Leibold, 2003). For
instance, resource partitioning among species has been
proposed to reduce competition and promote coexistence
within assemblages (Pianka, 1974; Schoener, 1974; Grant,
1986; Lossos etal., 1997; Farlow and Pianka, 2002). However, analyses have not explored how transformations of
vegetation cover type affect species association with specific microhabitats and change species composition and
diversity in the vegetation cover type.
The northern Andes of South America have several
heterogeneous landscapes combining forested and altered
areas where the negative effect of habitat transformation
on amphibian diversity (Gutirrez-Lamus et al., 2004;
Herrera etal., 2004; Garca etal., 2007, Mendez-Narvaez
2014) and specific association among species and their
vegetation cover type (Arroyo etal., 2003; Herrera-Montes etal., 2004; Cadavid etal., 2005; Garca etal., 2005;
Garca etal., 2007) have been demonstrated. However, to
our knowledge no studies have combined ecological approaches such as the components of biological diversity
and microhabitat use in order to understand the effect of
human activities on species diversity in altered landscapes.
Thus, this study attempted to study the species turnover
of anurans between altered and natural vegetation cover
types and evaluate their partitioning resources in the Cordillera de los Andes from Colombia. We hypothesized that
transformations of vegetation cover type have a negative
effect on amphibian alpha and beta diversity. We also hypothesized that niche partitioning and species preferences
differ between forested and human-altered areas.
MATERIALS AND METHODS
Study area and data collection
Amphibians were sampled at Reserva Forestal Protectora del Ro Bitaco and neighboring properties, Vereda
Chicoral, Municipality of La Cumbre, Valle del Cauca department, Colombia (0435N, 7704W, 17002100 m

above sea level). The study area is located in the middle

of the Cordillera Occidental of the Colombian Andes. It
belongs to the Mountain Forest of the Northwest Andes
ecoregion (WWF, 2015), which is characterized as a very
humid pre-montane tropical forest (Holdridge, 1967).
The average annual rainfall is 2,000mm, with an annual
temperature of 1418C. This region is typically characterized by two rainy seasons from MarchMay and OctoberNovember. More than 80% of the vegetation cover
of the forest reserve natural in the high and steep areas;
however, most of the accessible area is characterized by
secondary vegetation and, because of several headwaters,
riparian vegetation is abundant around the Bitaco river
(Arana, 2006).
We defined four main vegetation cover types according to vegetation composition, which we grouped in two
categories based on the process of vegetation cover transformation. The first group comprised the forested areas
categorized as Riparian Forest (RF) and Secondary Forest
(SF), whereas the second group comprised the humanaltered areas categorized as Tea Crop (TC) and Livestock
Area (LA). The RF was characterized by native vegetation
growing along stream edges, which have been protected
for the establishment of small protective zones, whereas
the SF was characterized by secondary vegetation, since
in the 1960s this area was subjected to logging (Arana
2006). Vegetation included some tall trees, shrub, and
ferns, but since tall trees are over-dispersed along the
stream, vegetation covert is not complete above the water
body. Dominant groups of vegetation include Rubiaceae,
Orchidaceae, Solanaceae, Lauraceae, Melastomataceae,
among other. On the other hand, the TC was a monoculture of ca.60ha >20 years old, composed of small shrubs
of 1.5m tall, whereas LA was characterized by herbaceous
vegetation dominated by grass and some small shrubs.
Fieldwork was conducted from August 2008January 2009, about 1 week per month. These include surveys
in both rainy and dry seasons, although during the latter light rains were common. We employed the technique
of Visual Encounter Survey (VES; Heyer et al., 1994) to
evaluate the species diversity. Surveys were carried out
by two researchers during the day (8:0011:00 h) and
night (18:0000:00h). For each observed individual, we
recorded the species identity, time of activity (diurnal or
nocturnal), vegetation cover, vertical stratification (0cm,
I=150cm, II=51100cm, III=101150cm, IV=151
200 cm, V 200 cm) and substrate (leaf litter, leaves,
branches, under rocks, grass, and bare soil) according to
the standard categories established by Heyer (1994). We
followed the taxonomy of the Amphibian Species of the
World (Frost, 2014). The total survey effort was 111 person hours (ph) for the entire landscape, with 30ph in
the SF, 35ph in the RF, 23ph in the TC, and y 23ph in
the LA. Less effort was made in human-altered areas since
their area was proportionally lower than in forested areas.

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

South American Journal of Herpetology, 11(1), 2016, 111

Data analysis
We used abundance frequency data from each vegetation cover type to calculate two types of rarefaction
(sample-size- and coverage-based) and extrapolation
curves of Hill numbers (Chao etal., 2014). We used Hill
numbers of three orders (qD) using the following equation:
q

D=

i =1

Pi q

1 /(1 q )

Where S is the number of species in the assemblage,

and the ith species has relative abundance Pi, i=1, 2, ,
S. The parameter q determines the sensitivity of the measure to the relative frequencies. When q = 0, the abundances of individual species do not contribute to the sum,
so only presences are counted, giving species richness
(0D); q=1 weighs species in proportion to their frequency,
giving the exponential Shannons entropy index (1D); and
q=2 places more weight on the frequencies of abundant
species and discounts rare species, giving the inverse of
Simpsons entropy index (2D). For each Hill number we
defined the expected diversity D(m) from the general rarefaction formula of any order q (Chao et al. 2014). The
extrapolation of Hill numbers of any order q is a prediction of the expected diversity qD(n+m*) for an augmented
sample of size m=n+m*.
q

D ( m) =

m
k =1

(k / m )q * f k (m )) 1 /(1q )

Where f k is the abundance frequency count of the

reference sample of size n (or the maximum number of
individuals), that is define for m1 as the number of species represented by exactly k individuals in a sample of
size m.
We plotted diversity accumulation curves for the expected species richness as a function of individual sample
size or as a function of sample coverage. The asymptote
of this curve as sample size tends to infinity is the species
richness in the entire assemblage (Chao etal., 2014). The
constructed sampled size-based curves were used to compare amphibian species diversities between the four vegetation cover types, which were compared using the confidence interval based on a bootstrap method (95%). We
also extrapolated up to double the reference sample size
for each vegetation cover type. There are significant differences at the level of 5% among the expected diversities,
if the 95% confidence intervals do not overlap. We linked
the sample-size based curves by a sample completeness
curve, which reveals the relationship between sample size
(number of individuals) and sample completeness. This
curve illustrates how much sampling effort is needed to
achieve a predetermined level of sample completeness.
All statistical analyses were performed in the package iNEXT (version 2.0.5), developed by Chao etal. (2015), in R
(RCoreTeam, 2015).

Species turnover between vegetation cover types

was assessed through complementarity values (C_AB).
The value of species complementary varies from 0, when
both sites are identical in species composition, to 1, when
both sites are entirely different (Colwell and Coddington,
1994).
We used Chi-square tests to evaluate the relation
between the vegetation cover type and species substrate
and vertical stratification preferences and the species
preferences for specific microhabitat categories. The resource partitioning in each vegetation cover type was
calculated with the value of niche overlapping between
species pairs (Ojk), following the mathematic formula proposed by Pianka (1973).

Oij = Okj =

P(ij ) P(ik )
P(ij ) P(ik )
2

Where Pij and Pik represent the proportion of the ith

resource used by the jth and the kth species.
We randomized our values of niche overlap for null
model analysis in the EcoSim package (version 0.1.0), developed by Gotelli and Ellison (2013), in R (RCoreTeam,
2015). This module of EcoSimR tests for overlap in resource use among a set of coexisting species using a set of
unordered, discrete resource categories. The analysis reveals whether the average niche overlap calculated among
all unique pairs of species is more or less than would be
expected if species used resource categories independently of one another.
The estimation of the niche breadth, B, was performed using the formula of reciprocal measure of Simpson (1949):

B = 1

( [( Pi) ])
2

Where i is the microhabitat category used, P is the

proportion of the i used by that species and n is the total
number of microhabitat categories
RESULTS
Landscape diversity
We recorded 14 species of frogs belonging to four
families and six genera (Table1). The family Craugastoridae accounted for the highest number of species (71.5%),
followed by Centrolenidae (14.3%), and Dendrobatidae
and Hylidae (7.1%, each). Pristimantis palmeri achieved
the highest relative abundance with 46.3% of the records,
followed by Pristimantis erythropleura with 16.17%, Pristi
mantis calcaratus with 8.92%, Dendropsophus columbianus
with 7.81% and Nymphargus ignotus with 6.50%.

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

South American Journal of Herpetology, 11(1), 2016, 111

Table 1. Amphibian species composition and relative frequencies by vegetation cover type in forested and human-altered areas of the Cordillera
Occidental, Colombia.
Species
DENDROBATIDAE
Colostethus fraterdanieli (Silverstone, 1971)
HYLIDAE
Dendropsophus columbianus (Boettger, 1892)
CENTROLENIDAE
Nymphargus ignotus (Lynch, 1990)
Centrolene savagei (Ruiz-Carranza and Lynch, 1991)
STRABOMANTIDAE
Hypodactylus mantipus (Boulenger, 1908)
Pristimantis juanchoi (Lynch, 1996)
Pristimantis palmeri (Boulenger, 1912)
Pristimantis calcaratus (Boulenger, 1908)
Pristimantis orpacobates (Lynch, Ruiz-Carranza and Ardila-Robayo, 1994)
Pristimantis brevifrons (Lynch, 1981)
Pristimantis erythropleura (Boulenger, 1896)
Pristimantis platychilus (Lynch, 1996)
Pristimantis permixtus (Lynch, Ruiz-Carranza and Ardila-Robayo, 1994)
Pristimantiscf.boulengeri (Lynch, 1981)
Total records/habitat

Vegetation cover type and turnover diversity

To compare diversities among each vegetation cover
type, we used each fixed value of q (q=0, 1, and 2), with
95% confidence intervals (parenthesis) at the reference
sample size (number of individual frogs) and a graphically extrapolated up to double the reference sample size
(Fig.1). Forested areas (RF and SF) had the highest values of diversity, with reference sample sizes of 163 and
204 for RF and SF respectively. The Hill numbers of order
q=0,1,2 for these reference sample size were estimated to
be 9 (8.049.95), 5.06 (4.415.72), and 3.59 (2.994.19),
respectively for the Riparian Forest, and 9 (7.7710.22),
4.69 (4.095.29), and 3.39 (2.833.95) for the Secondary

Secondary
forest

Riparian
forest

Tea crop

Livestock
area

Total
records/
species

0.06

0.69

0.02

42

0
0

0.21
0.09

0
0

0
0

35
14

0.06
0.02
0.47
0.17
0.04
0.03
0.16
0
0.04
0.01
204

0
0.01
0.46
0.08
0.05
0
0.03
0.01
0
0
163

0
0
0.31
0
0
0
0
0
0
0
58

0
0
0.55
0
0
0
0.43
0
0
0
113

13
6
249
48
16
6
87
2
5
3
538

Forest. Species diversity of order q=0 was the same in RF

and SF (Fig.1A). Species diversity of order q=1 and of
order q=2 were higher in RF than in SF (Fig.1B and 1C respectively), although there is almost complete overlap between the two confidence intervals. Human-altered areas
(LA and TC) had lower values of diversity for all Hill numbers compared to forested areas, with a reference sample
sizes of 115 and 58 for LA and TC respectively. The Hill
numbers of orders q=0,1,2, for these reference sample
size were estimated to be 3 (2.453.54), 2.13 (1.952.31),
and 2.03 (1.882.18), respectively, for LA, and 2, 1.85
(1.682.03), and 1.74 (1.492) for the TC. LA had higher
values of Hill numbers q=0, 1, and 2 than TC (Fig.1AC),
although the last two indices overlapped their confidence

Figure1. Comparison of sample-size-based rarefaction (solid lines) and extrapolation (dashed curves) of anuran species diversity in four vegetation
cover types for Hill numbers of order (A)q=0, (B)q=1, and (C)q=2. The 95% confidence intervals were obtained by a bootstrap method based on 200
replicates. Reference samples are denoted by solid dots.

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

South American Journal of Herpetology, 11(1), 2016, 111

that species diversities are significantly higher in forested

areas than in human-altered areas, for any standardized
sample coverage and also that our samples reached a complete coverage (Fig.3).
The species complementarity (turnover) between
vegetation cover types was highest between forested areas and human-altered areas. Among them, the highest
species complementarity was between both SF or RF and
TC (C_AB=0.90) and the lowest was between TC and LA
(C_AB = 0.33). The mean species complementarity was
high for the overall landscape diversity (C_AB=0.73).
Microhabitat choice and resource partitioning

Figure 2. Sample coverage for rarefied samples (solid line) and extrapolated samples (dashed line) as a function of sample size for anuran
samples from four vegetation cover types. The 95% confidence intervals
were obtained by a bootstrap method based on 200 replicates. Reference
samples are denoted by solid dots.

intervals (Fig. 1). Thus, forested areas had abundant,

common, and rare species, whereas human altered areas
had mainly abundant species (Table1).
Anuran representation reached 99100% as a function of sample size in each vegetation cover type at the
reference sample sizes, without any significant increase
beyond these values (Fig. 2). The sample completeness
curve showed an asymptote with a lower sample size in
human-altered areas than in forested areas. For any fixed
sample size <60 sample units, the sample coverage for the
RF and SF is significantly lower than coverage in TC and
LA. To compare diversities among each vegetation cover
type for all Hill numbers (q = 0, 1, 2), we presented for
each area the coverage-based rarefaction and extrapolation curves with 95% confidence intervals. Because the
increase in coverage for the extrapolation is small, it is not
possible to see any increment in this figure. We confirmed

Leaves and branches were used as substrate by most

species, followed by leaf litter, grass, and bare soil. The
highest proportion of individuals was recorded on leaves
(73.61%), followed by branches (13.94%), leaf litter
(7.99%), bare soil (2.97%), and grass (1.49%). Stratum III
was used by most of the species as vertical stratification,
while the lowest number of species was recorded in the
strata 0 and I. The highest proportion of individuals was
recorded between stratum I and III (69.33%), followed by
stratum IV (15.05%), stratum 0 (10.96%) and stratum
V (4.65%). Nocturnal activity was exhibited in 13 of 14
species and just three species presented diurnal activity.
Similarly, 92.4% of the individuals being recorded at night
(Table2).
There was a significant association between vegetation cover type and substrate (Chi2 = 42.07, P < 0.001,
df = 12): both, leaves and branches were the substrate
used in all the vegetation cover types, but grass, in forested areas, and leaf litter, in human-altered areas, were not
used by any individual (Fig.4). Also, there was a significant association between the vegetation cover type and
vertical stratification (Chi2=141.63, P<0.001, df=15):
all the strata were used in the forested areas, but in

Figure3. Comparison of coverage-based rarefaction (solid lines) and extrapolation (dashed lines) of anuran diversity in four vegetation cover types for
Hill numbers of order (A)q=0, (B)q=1, and (C)q=2. The 95% confidence intervals were obtained by a bootstrap method based on 200 replicates.
Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

South American Journal of Herpetology, 11(1), 2016, 111

Table 2. Substrate, vertical stratification, and activity associations of the anuran assemble in forested and human-altered areas of the Cordillera
Occidental, Colombia. Significant association between a species and the substrate or vertical stratification is denoted by one asterisk(*) and between a
species and both categories by two asterisks(**). See Results for details. Substrate: leaf litter =Ll; leaves =L; branches =B; under rocks =Ur; grass =G;
and bare soil =Bs. Stratum: 0; I=150cm; II=51100cm; III=101150cm; IV=151200cm y V200cm. Activity: Diurnal =Di, Nocturnal =No.
Species
Pristimantis palmeri*
Pristimantis erythropleura*
Pristimantis brevifrons
Hypodactylus mantipus*
Pristimantis juanchoi
Pristimantis calcaratus*
Pristimantis orpacobates**
Pristimantis platychilus
Pristimantis permixtus
Pristimantiscf.boulengeri
Nymphargus ignotus*
Centrolene savagei*
Dendropsophus columbianus*
Colostethus fraterdanieli
Total

Ll
20
0
0
13
0
0
1
0
0
0
0
0
0
9
43

L
176
76
5
0
5
34
10
2
8
2
35
14
29
0
396

B
37
9
1
0
0
11
5
0
0
1
0
0
11
0
75

Substrate
Ur
G
0
4
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
0
0
0
8

human-altered areas, individuals were found commonly

between strata 0 and III (Fig.4).
Species with >10 records were used to test species
association by substrates and stratifications. Pristiman
tis palmeri showed a significant association with leaves
and strata IIII (Chi2=543.89, P<0.001; Chi2=68.71,
P<0.001), P.erythropleura with leaves and strata I and II
(Chi2=317.20, P<0.001; Chi2=54.59, P<0.001), P.calca
ratus with leaves and strata IIIV (Chi2=112.75, P<0.001;
Chi2 = 13, P = 0.02), P. orpacobates with leaves and no
association with any stratum (Chi2 = 31.25, P < 0.001;
Chi2 = 3.50, P = 0.62), Hypodactylus mantipus with leaf

Bs
12
0
0
0
1
3
0
0
0
0
0
0
0
0
16

0
30
0
0
13
1
3
1
0
0
0
0
0
2
9
59

I
63
29
0
0
1
6
4
0
1
0
0
0
10
0
114

II
73
27
0
0
1
12
1
0
3
2
10
0
10
0
139

Stratum
III
43
19
1
0
1
13
3
1
1
0
17
1
20
0
120

IV
33
11
3
0
0
11
4
1
1
0
8
8
0
0
81

V
7
1
2
0
2
3
3
0
1
1
0
5
0
0
25

Activity
Di
No
28
221
0
87
0
6
4
9
0
6
0
48
0
16
0
2
0
8
0
3
0
35
0
14
0
42
9
0
41
497

litter and stratum 0 (Chi2 = 65, P < 0.001; Chi2 = 65,

P<0.001), Nymphargus ignotus with leaves and strata II
and III (Chi2=175, P<0.001; Chi2=42.66 P<0.001), Cen
trolene savagei with leaves and strata IV and V (Chi2=65,
P<0.001; Chi2=24.38, P<0.001), and Dendropsophus co
lumbianus with leaves and strata IIII (Chi2=96, P<0.001;
Chi2=44.28, P<0.001).
The niche overlap between species in each vegetation cover type showed that for substrate all vegetation
cover types had higher observed index than expected by
simulation, being outside of the confidence interval for
the set of simulated matrices (1000 times), although

Figure4. Association between kind of habitat and substrate (Left) or vertical stratum (Right) in the anuran community.

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

South American Journal of Herpetology, 11(1), 2016, 111

Figure5. Resource overlapping in microhabitat use, for (A)substrate and (B)stratum among anuran species in four different vegetation cover types
showing the histogram of the simulated index values (blue bars), observed index value (red vertical line), and one- and two-tailed 95% confidence intervals (pairs of black vertical thin-dashed and thick-dashed lines, respectively) for Secondary Forest (SF), Riparian Forest (RF), Livestock Area (LA), and
Tea Crop (TC).

observed index and the mean of simulated index are farther in forested than in human-altered areas (Fig. 5A).
For stratum, the observed index of niche overlap fell into
the confidence interval for FI, RF and TC but not for LA
(Fig.5B). Observed and simulated values (in parenthesis)
of niche overlap for substrate were estimated to be lower
in SF and RF, 0.75 (0.22) and 0.71 (0.21) respectively,
than in TC and LA, 0.94 (0.26) and 0.78 (0.30) respectively. For stratum, observed values but not simulated for
niche overlap were estimated to be lower in SF and RF,
0.52 (0.53) and 0.38 (0.42) respectively, than in TC and

LA, 0.62 (0.45) and 0.89 (0.33). The niche breadth average was similar among vegetation cover types: P.palmeri
had the highest niche breadth, followed by P.erythropleura
and P.permixtus (Table3).
DISCUSSION
The species diversity was influenced by the vegetation cover type, with higher species richness in forestedareas than in human-altered areas. The highest species

Table3. Niche breadth values of the anuran species in each vegetation cover type and mean niche breadth value by vegetation cover type. An asterisk (*)
denotes absence of the species.
Species
Pristimantis palmeri
Pristimantis erythropleura
Pristimantis brevifrons
Hypodactylus mantipus
Pristimantis juanchoi
Pristimantis calcaratus
Pristimantis orpacobates
Pristimantis permixtus
Pristimantis platychilus
Nymphargus ignotus
Centrolene savagei
Colostethus fraterdanieli
Dendropsophus columbianus
Breadth

Secondary Forest
0.76
0.72
0.72
0.5
0.76
0.81
0.71
0.69
*
*
*
*
*
0.78

Riparian Forest
0.85
0.64
*
*
0.63
0.74
0.82
*
0.63
0.66
0.63
0.50
*
0.68

Tea Crop
0.68
*
*
*
*
*
*
*
*
*
*
*
0.77
0.72

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

Livestock Area
0.80
0.72
*
*
*
*
*
*
*
*
*
*
0.63
0.72

Mean Breadth/habitat
0.77
0.69
0.72
0.5
0.70
0.78
0.77
0.69
0.63
0.66
0.63
0.50
0.7

South American Journal of Herpetology, 11(1), 2016, 111

turnover was between forested areas and human-altered

areas; but the former had a higher number of unique species. Also, the species in the community showed specific
microhabitat associations with the substrate and the vertical stratification, with higher mean values of niche overlap between species pairs in the human-altered areas than
forested-area. Both sources of evidence suggest an effect
of vegetation cover type and microhabitat characteristics
(vegetation cover type transformation and microhabitat
availability) on species diversity, which is evident from
both the decrease in the species number and the increase
in the overlap between species in human-altered areas.
Our anuran species account followed the same taxonomic dominance of amphibian families reported in previous species inventories in the Northern Andes of Colombia (see Arroyo et al., 2003; Gutirrez-Lamus et al.,
2004; Herrera-Montes etal., 2004; Cadavid etal., 2005;
Garca etal., 2007; Bernal and Lynch, 2008). The inventory representation of species reached between 99% and
100% in this study, but compared with historical records
in the region (Bolivar-G. etal., 2010) there was a reduction of almost 50% in anuran species richness: 14 of 29
historically recorded species. It seems that the number of
species in the region has been declining over time periods,
where the last two periods (BolivarG. etal., 2010; Herrera, 2007) showed most similarity in species composition.
Nonetheless, we highlight the new record of P.permixtus
(Mndez-Narvez etal., 2010) for Valle del Cauca and the
presence of P. cf. boulengeri and P. platychilus. Interestingly, P.platychilus has been recorded few times in Valle
del Cauca and unrecorded in the locality for more than 15
years (Castro etal., 2004). The absent species are listed in
some categories of threat of the IUCN and national list of
endangered species, and most of them are characterized
by their large size and association with riparian vegetation cover types (BolvarG. etal., 2010). It has been suggested that this morphological and ecological association
(ecotype) experiences the most drastic processes of physiological stress due to vegetation cover type transformation (Pineda and Halffter, 2005).
Population declines of a similar order of magnitude
have been reported in other highland locations in Ecuador, Mexico, Panama, and Peru, mainly associated with
epidemic diseases (Lips et al., 2004; Bustamante et al.,
2005; Crawford etal., 2010; Catenazzi etal., 2011). Here,
we showed that the vegetation cover type transformation
might have caused the considerable decrease in the current number of species from 93, even comparable with
the historical estimate. This cause is considered one of
the main threats to amphibian populations (Stuart etal.,
2008). Although the high mean species complementarity
between vegetation cover type (73%) might suggest high
overall species diversity in the region and different species composition between vegetation cover type, in human-altered areas we found a lower proportion of species

compared with the overall diversity (20%) than in forested areas (93%, Table1). Moreover, forested areas, despite
having attained high species complementarity (RF and
SF=62%), had several unique species, whereas in humanaltered areas D.columbianus was the only unique species,
which is a common species in open areas and tolerant to
processes of vegetation cover type transformations (Estupian and Galatti, 1999; Bolivar and Renjifo, 2004).
An important consequence of the vegetation cover
type transformation is the loss of essential microhabitat
for the survival and reproduction of individuals (RuedaAlmonacid et al., 2004). The interaction among species
and between them and their environment delimit the
species niche (Shmida and Wilson, 1985). Thus, species
association with specific microhabitats might also imply
an association with a particular vegetation cover type and
impact their survival. We had two sources of evidence to
support this hypothesis. First, we found a significant association between the use of particular substrates and
vertical stratification and the vegetation cover type. We
also found a significant association between some species
with either the substrate or vertical stratification.
Transformation of vegetation cover type has been
proposed to change microhabitat preferences in other vertebrates like reptiles (Luiselli, 2006; Luiselli etal., 2006)
and birds (Franzreb, 1983). It also has been suggested to
affect landscape diversity, with an inverse relationship
between the number of species in an assembly and the
degree of niche overlap (Pianka, 1974). Our results also
support this idea, since the human-altered areas had the
highest level of niche overlap with lower microhabitat
availability and species richness than forested areas.
Species with high niche breath are considered excellent to colonize or resist environmental transformations
(Heyer and Bellin, 1973; Swihart etal., 2002). Our results
supported this idea since Pristimantis palmeri and P.ery
trhopleura showed high niche breadth and were present
in both forested and human-altered areas. Nonetheless,
P.calcaratus, P.orpacobates, and P.brevifrons also showed
high values of niche breadth and were only distributed in
forested areas. Other niche dimensions such as diet, morphological and physiological characteristics, and specific
breeding sites might be important in resources partitioning among species (Toft, 1985; Heyer et al., 1990; Lima
and Magnusson, 1998; Muoz-Guerrero etal., 2007; Santos and Rossa-Feres, 2007; Vasconcelos and Rossa-Feres,
2008; Mndez-Narvaez etal., 2015).
In summary, this study showed the negative effect
of human vegetation cover type transformation of Andean ecosystems on local species richness, species turnover, and resource preferences by amphibians, using for
first time complementary ecological approaches such as
components of biological diversity and species niche preferences and overlap. The absence of several species in
human-altered vegetation cover types could be an effect

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

South American Journal of Herpetology, 11(1), 2016, 111

of the elimination of some microhabitats in these transformations. Thus, the inclusion of ecological information
like species microhabitat associations in surveys of species diversity can provide a better understanding of particular causes for the species loss from landscape changes.
In fact, the limited information of the natural history in
amphibians has made the assessment of the conservation
status of several species a major challenge (Rueda-Almonacid, 2004).
ACKNOWLEDGMENTS
We would like to thank the communal action board
of Chicoral, especially to Margot Albear, Don Jorge Albear, and their son Diego Albear, who provided accommodation in their house during the field work. We also thank
biologists Laura Tabares, Jhon Jairo Ospina, Jimmy Cabra, and Carim Lpez for their help during fieldwork, and
to Carolina Amorocho for comments in the manuscript
and improvement of English.
REFERENCES
Acosta-Galvis A. 2000. Ranas, salamandras y caecilias (Tetrapoda:
Amphibia) de Colombia. Biota Colombiana 1:289319.
Alford R.A., Richards S.J. 1999. Global amphibian declines: a
problem in applied ecology. Annual Review of Ecology, Evolution, and
Systematics 30:133165. doi:10.1146/annurev.ecolsys.30.1.133
Alford R.A., Bradfield K.S., Richards S.J. 2007. Global warming and
amphibian losses. Nature 447:E34. doi:10.1038/nature05940
Angulo A., Rueda-Almonacid J.V., Rodriguez-Mahecha J.V.,
La Marca E. 2006. Tcnicas de Inventario y Monitoreo para los
Anfibios de la Regin Tropical Andina. Conservacin internacional.
Serie de Manuales de Campo N2. Panamericana Formas e Impresos
S.A., Bogot.
Arana A.E. 2006. Plan de Manejo Participativo Reserva Forestal de
Bitaco. Corporacin Autnoma Regional del Valle del Cauca, CVC
Direccin Tcnica Ambiental Grupo de Biodiversidad, Cali.
Arroyo S., Jerez A., Ramrez-Pinilla M.P. 2003. Anuros de un bosque
de niebla de la cordillera oriental de Colombia. Caldasia 25:153167.
Bernal M.H., Lynch J.D. 2008. Review and analysis of altitudinal
distribution of the Andean anurans in Colombia. Zootaxa 1826:1
25. doi:10.11646/zootaxa.1826.1.1
Blaustein A.R., Wake D.B., Sousa W.P. 1994. Amphibian declines:
judging stability, persistence, and susceptibility of populations
to local and global extinctions. Conservation Biology 8:6071.
doi:10.1046/j.1523-1739.1994.08010060.x
Boettger O. 1892. Katalog der Batrachier-Sammlung im Museum der
Senckenbergischen Naturforschenden Gesellshaft in Frankfurt am
Main. Frankfurt a. M.: Gebrder Knauer.
Bolvar W., Renjifo J.M. 2004 Dendropsophus columbianus The IUCN
Red List of Threatened Species. Version 2014.2. Accessible at www.
iucnredlist.org
BolvarG W., Eusse Gonzlez D., Castro Herrera F., Fierro
Caldern K., Cifuentes Sarmiento Y., Falk Fernndez P.,
Neira L.A. 2010. Aves y Herpetos de la Reserva Forestal Protectora
Regional de Bitaco. Corporacin Autnoma Regional del Valle Del
Cauca (CVC), Cali.
Boulenger G.A. 1896. Descriptions of new reptiles and batrachians
from Colombia. Annals and Magazine of Natural History 17:1621.

Boulenger G.A. 1908. Descriptions of new batrachians and reptiles

discoverd by Mr. M.G. Palmer in south-western Colombia. Annals
and Magazine of Natural History 2:515522.
Boulenger G.A. 1912. Descriptions of new batrachians from the Andes
of South America, preserved in the British Museum. Annals and
Magazine of Natural History, Series 8 10:185191.
Bustamante M.R., Ron S.R., Coloma L.A. 2005. Cambios en la
diversidad en siete comunidades de anuros en los Andes de Ecuador.
Biotropica 37:180189. doi:10.1111/j.1744-7429.2005.00025.x
Cabrera E., Vargas D.M., Galindo G., Garca M.C., Ordoez M.F.,
Vergara L.K., Giraldo Y.P. 2011. Memoria Tcnica de la
Cuantificacin de la Deforestacin Histrica Nacional Escalas
Gruesa y Fina. Instituto de Hidrologa, Meteorologa, y Estudios
Ambientales-Ideam, Bogot.
Cadavid J.G., Roman-Valencia C., Gomez A.F. 2005. Composicin
y estructura de anfibios anuros en un transecto altitudinal de los
Andes centrales de Colombia. Revista del Museo Argentino de Ciencias
Naturales 7:103118.
Castro F., Herrera M.I., Lynch J.D. 2004. Pristimantis platychilus. The
IUCN Red List of Threatened Species. Version 2014.2. Accessible at
www.iucnredlist.org.
Catenazzi A., Lehr E., Rodriguez L.O., Vredenburg V.T. 2011.
Batrachochytrium dendrobatidis and the collapse of anuran
species richness and abundance in the upper Manu National
Park, southeastern Peru. Conservation Biology 25:382391.
doi:10.1111/j.1523-1739.2010.01604.x
Chao A., Gotelli N.J., Hsieh, T.C., Sander E.L., Ma K.H., Colwell
R.K., Ellison A.M. 2014. Rarefaction and extrapolation
with Hill numbers: a framework for sampling and estimation
in species diversity studies. Ecological Monographs 84:4567.
doi:10.1890/13-0133.1
Chao A., Ma K.H., Hsieh T.C. 2015. SpadeR: Species Prediction and
Diversity Estimation with R. R Package Version 0.1.0. Available
from: http://chao.stat.nthu.edu.tw/blog/software-download
Collins J.P., Storfer A. 2003. Global amphibian declines:
sorting the hypotheses. Diverssity and Distribution 9:8998.
doi:10.1046/j.1472-4642.2003.00012.x
Condit R., Pitman N., Leigh E.G., Chave J., Terborgh J., Foster
R.B., Hubbell S.P. 2002. Beta-diversity in tropical forest trees.
Science 295:666669. doi:10.1126/science.1066854
Crawford A.J., Lips K.R., Berminhgam E. 2010. Epidemic disease
decimates amphibian abundance, species diversity, and evolutionary
history in the highlands of central Panama. Proceedings of the
National Academy of Sciences USA 107:1377713782. doi:10.1073/
pnas.0914115107
Estupian R.A., Galatti U. 1999. La fauna anura en reas con
diferentes grados de intervencin antrpica de la amazonia oriental
brasilea. Revista de la Academia Colombiana de Ciencias Naturales y
Exactas 23:275286.
Farlow J.O., Pianka E.R. 2002. Body size overlap, habitat partitioning
and living space requirements of terrestrial vertebrate predators:
implications for the paleoecology of large theropod dinosaurs.
Historical Biology 16:2140.
Foden W.B., Butchart S.H., Stuart S.N., Vi J.C., Akakaya
H.R., Angulo A., S.D. Donner 2013. Identifying the worlds
most climate change vulnerable species: a systematic trait-based
assessment of all birds, amphibians and corals. PLoS One 8:e65427.
doi:10.1371/journal.pone.0065427
Franzreb K.E. 1983. A comparison of avian foraging behavior in
unlogged and logged mixed-coniferous forest. Wilson Library
Bulletin 95:6076.
Frost D.R. 2015. Amphibian species of the world: an online reference.
Version 5.6 (9 January 2013). Accessible at http://research.amnh.
org/herpetology/amphibia/index.html
GarcaR. J.C., CastroH. F., CrdenasH. H. 2005. Relacin entre la
distribucin de anuros y variables del hbitat en el sector la Romelia
del Parque Nacional Natural Munchique (Cauca, Colombia). Caldasia
27:299310.

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

South American Journal of Herpetology, 11(1), 2016, 111

Garca J.C., CrdenasH H., CastroH F. 2007. Relacin entre la

diversidad de anuros y los estados sucesionales de un bosque muy
hmedo montano bajo del valle del cauca, suroccidente colombiano.
Caldasia 29:363374.
Gotelli N.J. Ellison A.M. 2013. EcoSimR: Null Models For Ecology.
Version 1.00 (15 June 2013). Available from: www.uvm.
edu/~ngotelli/EcoSim/EcoSim.html
Guarnizo C.E., Paz A., Muoz-Ortiz A., Flechas S.V., MndezNarvez J., Crawford A.J. 2015. DNA barcoding survey of
anurans across the Eastern Cordillera of Colombia and the impact of
the Andes on cryptic diversity. PloS One 10:e0127312. doi:10.1371/
journal.pone.0127312
Gutirrez-Lamus D.L., Serrano V.H., Ramrez-Pinilla M.P. 2004.
Composicin y abundancia de anuros en dos tipos de bosque
(natural y cultivado) en la cordillera oriental colombiana. Caldasia
26:245264.
Halffter G., Moreno C.E. 2005. Significado biolgico de las
diversidades Alfa, Beta Y Gamma. Pp. 518, in Halffter G.J.,
Sobern P., Koleff P., Melic A. (Eds.) Sobre Diversidad Biolgica: El
Significado De La Diversidad Alfa, Beta Y Gamma. SEA, CONABIO,
Grupo DIVERSITAS and CONACYT, Zaragoza.
Hamilton L.S. 1995. Mountain cloud forest conservation and research:
a synopsis. Mountain Research and Development 15:259266.
doi:10.2307/3673933
Herrera, M.I. 2007. Anlisis multitemporal de la riqueza de
herepetofauna en un transecto de bosque de niebla (ChicoralKM18-Bosque de San Antonio) en el departamento del Valle del
Cauca, Suroccidente Colombiano. Undergraduate Dissertation,
Universidad del Cauca, Colombia.
Herrera-Montes A., Olaya L.A., Castro F. 2004. Incidencia de la
perturbacin antrpica en la diversidad, la riqueza y la distribucin
de Eleutherodactylus (Anura: Leptodactylidae) en un bosque nublado
del suroccidente colombiano. Caldasia 26:265274.
Heyer W.R., Bellin M.S. 1973. Ecological notes on five sympatric
Leptodactylus (Amphibia: Leptodactylidae) from Ecuador.
Herpetologica 29:6672.
Heyer W.R., Rand A.S., Cruz C.A.G., Peixoto O.L., Nelson C.E.
1990. Frogs of Boracia. Arquivos de Zoologia 31:231410.
Holdridge, L.R. 1967. Life Zone Ecology, 2nd ed. Tropical Science Center, San Jos.
Hutchinson G.E. 1957. Concluding remarks. Cold Spring Harbor
Symposia on Quantitative Biology 22:415427. doi:10.1101/
SQB.1957.022.01.039
Hutter C.R., Guayasamin J.M., Wiens J.J. 2013. Explaining Andean
megadiversity: the evolutionary and ecological causes of glassfrog
elevational richness patterns. Ecology Letters 16:11351144.
doi:10.1111/ele.12148
Kattan G.H., Alvarez-Lopez H. 1996. Preservation and management
of biodiversity in fragmented landscapes in the Colombian Andes.
Pp. 318, in Schelhas J., Greenberg R. (Eds.). Forest Patches in
Tropical Landscapes. Island Press, Washington D.C.
Kattan G.H., Franco P., Rojas V., Morales G. 2004. Biological
diversification in a complex region: a spatial analysis of faunistic
diversity and biogeography of the Andes of Colombia. Journal of
Biogeography 31:18291839. doi:10.1111/j.1365-2699.2004.01109.x
Kieswetter C.M., Schneider C.J. 2013. Phylogeography in the
northern Andes: complex history and cryptic diversity in a
cloud forest frog, Pristimantis wnigrum (Craugastoridae).
Molecular Phylogenetics and Evolution 69:417429. doi:10.1016/j.
ympev.2013.08.007
La Marca, E., Lips K.R., Ltters S., Puschendorf R.,
Ibaez R., Rueda-Almonacid J.V., Young B.E. 2005.
Catastrophic population declines and extinctions in Neotropical
Harlequin frogs (Bufonidae: Atelopus). Biotropica 37:190201.
doi:10.1111/j.1744-7429.2005.00026.x
Lima A.P., Magnusson W.E. 1998. Partitioning seasonal time:
interations among size, foraging activity and diet in leaf-litter frogs.
Oecologia 116:259266. doi:10.1007/s004420050587

10

Lips K.R., Mendelson J.R. III, Munoz-Alonso A., CansecoMrquez L., Mulcahy D.G. 2004. Amphibian population
declines in montane southern Mexico: resurveys of historical
localities. Biological Conservation 119:555564. doi:10.1016/j.
biocon.2004.01.017
Lips K.R., Burrowes P.A., Mendelson J.R., Parra-Olea G. 2005a.
Amphibian declines in Latin America: widespread population
declines, extinctions, and impacts. Biotropica 37:163165.
doi:10.1111/j.1744-7429.2005.00023.x
Lips K.R., Burrowes P.A., Mendelson J.R., Parra-Olea G. 2005b.
Amphibian population declines in Latin America: synthesis.
Biotropica 37:222226. doi:10.1111/j.1744-7429.2005.00029.x
Losos J.B. 1997. Adaptative differentiation following experimental
island colonization in Anolis lizards. Nature 387:7073.
doi:10.1038/387070a0
Luiselli L. 2006. Food niche overlap between sympatric potential
competitors increases with habitat alteration at different trophic
levels in rain-forest reptiles (omnivorous tortoises and carnivorous
vipers. Journal of Tropical Ecology 22:695704. doi:10.1017/
S0266467406003634
Luiselli L., Akani G.C., Politano E. 2006. Effects of habitat
alteration caused by petrochemical activities and oil spills on the
habitat use and interspecific relationships among four species of
afrotropical freshwater turtles. Pp.383399, in Hawksworth D.L.,
Bull A.T. (Eds.), Marine, Freshwater, and Wetlands Biodiversity
Conservation. Springer, Dordrecht.
Lynch J.D. 1981. Two new species of Eleutherodactylus from western
Colombia (Amphibia: Anura: Leptodactylidae). Occasional Papers of
the Museum of Zoology, University of Michigan 697:112.
Lynch J.D. 1990. A new ocellated frog (Centrolenidae) from western
Colombia. Proceedings of the Biological Society of Washington
103:3538.
Lynch J.D. 1996. New frogs of the genus Eleutherodactylus (family
Leptodactylidae) from the San Antonio region of the Colombian
Cordillera Occidental. Revista de la Academia Colombiana de Ciencias
Exactas, Fsicas y Naturales 20:331345.
Lynch J.D. 1998. La riqueza de la fauna anfibia de los Andes
colombianos. Innovacin y Ciencia 7:4651.
Lynch J.D., P.M. Ruiz-Carranza, and M.C. Ardila-Robayo.
1994. The identities of the Colombian frogs confused with
Eleutherodactylus latidiscus (Boulenger) (Amphibia: Anura:
Leptodactylidae). Occasional Papers of the Museum of Natural History,
University of Kansas 170:142.
Lynch J.D., Ruiz-Carranza P.M., Ardila-Robayo M.C. 1997.
Biogeographic patterns of Colombian frogs and toads. Revista de
la Academia Colombiana de Ciencias Naturales y Exactas 21:237248.
Marsh D.M., Pearman P.B. 1997. Effects of habitat fragmentation
on the abundance of two Species of leptodactylid frogs in an
Andean montane forest. Conservation Biology 11:13231328.
doi:10.1046/j.1523-1739.1997.95519.x
May R.M. 1975. Patterns of species abundance and diversity. Pp.81
120, in Cody M.L., Diamond J.M. (Eds.), Ecology and Evolution of
Communities. Harvard University Press, Cambridge.
Mndez-Narvez J. 2014. Diversidad de anfibios y reptiles en
hbitats altoandinos y paramunos de la cuenca del ro Fquene,
Cundinamarca, Colombia. Biota Colombiana 15:94103
Mndez-Narvez J., BolivarG. W., CastroH. F. 2010. Amphibia,
Anura, Strabomantidae, Pristimantis permixtus Lynch, RuizCarranza, and Ardila-Robayo, 1994: Distribution extension, Valle
del Cauca, Colombia. Check List 6:499500.
Mndez-Narvez J., Flechas S.V., Amzquita A. 2015. Foam nests
provide context-dependent thermal insulation to embryos of three
leptodactylid frogs. Physiological and Biochemical Zoology 88(3):246
253. doi:10.1086/680383
Moreno C.E. 2001. Mtodos para Medir la Biodiversidad. MandT
Manuales y Tesis SEA, Zaragoza.
Muoz-Guerrero J., Serrano V.H., Ramrez Pinilla M.P. 2007.
Uso de microhbitat, dieta y tiempo de actividad en cuatro especies

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

South American Journal of Herpetology, 11(1), 2016, 111

simptricas de ranas hlidas neotropicales (Anura: Hylidae). Caldasia

29:413425.
Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca G.A.B.,
Kent J. 2000. Biodiversity hotspots for conservation priorities.
Nature 403:853858. doi:10.1038/35002501
Navas C.A. 2003. Herpetological diversity along Andean elevational
gradients: links with physiological ecology and evolutionary
physiology. Comparative Biochemistry and Physiology A. 133:469
485. doi:10.1016/S1095-6433(02)00207-6
Navas C.A. 2006. Patterns of distribution of anurans in high Andean
tropical elevations: Insights from integrating biogeography and
evolutionary physiology. Integrative and Comparative Biology 46:82
91. doi:10.1093/icb/icj001
Pearman P.B. 1997. Correlates of Amphibian Diversity in an Altered
Landscape of Amazonian Ecuador. Conservation Biology 11:1211
1225. doi:10.1046/j.1523-1739.1997.96202.x
Pianka E.R. 1974. Niche Overlap and Diffuse Competition. Proceedings
of the National Academy of Sciences USA 71:21412145. doi:10.1073/
pnas.71.5.2141
Pineda E., Halffter G. 2004. Species diversity and habitat
fragmentation: frogs in a tropical montane landscape in
Mexico. Biological Conservation 117:499508. doi:10.1016/j.
biocon.2003.08.009
Pineda E., Moreno C., Escobar F., Halffter G. 2005. Frog,
bat and dung beetle diversity in the cloud forest and coffee
agrosystems of Veracruz, Mexico. Conservation Biology 19:400410.
doi:10.1111/j.1523-1739.2005.00531.x
Pounds J.A., Bustamante M.R., Coloma L.A., Consuegra J.A.,
Fogden M.P.L., Foster P.N., Young B.E. 2006. Widespread
amphibian extinctions from epidemic disease driven by global
warming. Nature 439:161167. doi:10.1038/nature04246
Pullian H.R. 2000. On the relationship between niche and distribution.
Ecology Letters 3:349361. doi:10.1046/j.1461-0248.2000.00143.x
R Core Team (2015). R: A language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna,
Austria. Available from: https://www.R-project.org

Rueda-Almonacid J.V., Lynch J.D., Amzquita A. 2004. Libro

Rojo de los Anfibios de Colombia. Serie Libros Rojos de Especies
Amenazadas de Colombia. Conservacin Internacional Colombiana,
Instituto De Ciencias Naturales Universidad Nacional de Colombia,
Ministerio del Medio Ambiente, Bogot.
Ruiz-Carranza P.M., Lynch J.D. 1991. Ranas Centrolenidae de
Colombia III. Nuevas especies de Cochranella del grupo granulosa.
Lozania 59:118.
Santos T.G., Rossa-Feres D.C. 2007. Similarities in calling site and
advertisement call among anuran amphibians in southeastern
Brazil. South American Journal of Herpetology 2:1730.
doi:10.2994/1808-9798(2007)2[17:SICSAA]2.0.CO;2
Schoener T.W. 1974. Resource partitioning in ecological communities.
Science 185:2739. doi:10.1126/science.185.4145.27
Shmida A., Wilson M.V. 1985. Biological determinants of species
diversity. Journal of Biogeography 12:120. doi:10.2307/2845026
Silverstone P.A. 1971. Status of certain frogs of the genus Colostethus,
with descriptions of new species. Natural History Museum of Los
Angeles County, Contributions in Science 215:18.
Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodriguez
A.S.L., Fischman D.L., Waller R.W. 2004. Status and trends of
amphibian declines and extinctions worldwide. Science 306:1783
1786. doi:10.1126/science.1103538
Stuart S.N., Hoffmann M., Chanson J.S., Cox N.A., Berridge R.J.,
Ramani P., Young B.E. 2008. Threatened Amphibians of the
World. Lynx Edicions, Barcelona.
Swihart R.K., Gehring T.M., Kolozsvary M.B., Nupp T.E. 2002.
Responses of resistant vertebrates to habitat loss and fragmentation:
the importance of niche breadth and range boundaries. Diversity
and Distribution 9:118. doi:10.1046/j.1472-4642.2003.00158.x
Tilman D. 2004. Niche tradeoffs, neutrality, and community structure:
A stochastic theory of resource competition, invasion, and
community assembly. Proceedings of the National Academy of Sciences
USA 101:1085410861. doi:10.1073/pnas.0403458101
Toft C.A. 1985. Resource partitioning in amphibians and reptiles.
Copeia 1985:121. doi:10.2307/1444785

Complementary Ecological Approaches to Understand Decreases in Frog Diversity in Altered Andean Ecosystems
Javier Mndez-Narvez, Wilmar BolvarG

View publication stats

11