Content uploaded by Sergio Estrada-Villegas
Author content
All content in this area was uploaded by Sergio Estrada-Villegas on Nov 09, 2014
Content may be subject to copyright.
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
1
Bats of Casanare, Colombia
Sergio Estrada-Villegas1,2,* and Beatriz H. Ramírez3
1 Asociación de Becarios de Casanare-ABC. Calle 17#15-55, Yopal, Casanare, Colombia. Tel. +57 (8)
6358938.
2 Programa para la Conservación de los Murciélagos de Colombia PCMCo. Calle 95 No. 17-37 Of. 104
Bogotá, Colombia. Tel. +57 (1) 6106051.
3 Centro de Estudios Ambientales de la Orinoquia CEAO - Asociación de Becarios de Casanare
* Corresponding author: estradavillegassergio@yahoo.com
ARTICLE
Manuscript history:
Submitted in 31/May/2012
Accepted in 26/Jun/2013
Available on line in 26JSep/2014
Editors: Marco A.R. Mello and
Valéria C. Tavares
Abstract
Colombia is known for its high bat richness, but regions like
Orinoquía remain poorly known for this group. Here we present
results from seven biodiversity assessments in Casanare, Colombia, a
department circumscribed within Orinoquía. We captured 1,116
individual bats of 51 species and five families. Desmodus rotundus,
Carollia spp., and Artibeus spp. were the most abundant taxa
sampled. We also captured elusive species such as Lampronycteris
brachyotis and Sphaeronycteris toxophyllum. In general, sites with
some sort of protection, lower in elevation, and towards the
southwest tended to have richer assemblages with different
composition than sites without protection, higher in elevation, and
towards the northeast of our study area. This southwest-northeast site
distribution follows a rainfall gradient, which might explain
differences in bat composition among sites. Finally, we discuss our
species list in light of others that have been published and present the
first analysis of assemblage structure for the bats of Casanare using
true diversities.
Keywords: Rényi diversity plot, true diversities, Orinoco basin,
elevational gradient, diversity, Desmodus rotundus, Phyllostomidae,
local communities.
!
Introduction
Colombia is known to harbor one of the richest
bat faunas in the world (Alberico et al. 2000) and
the richest phyllostomid assemblage in the
Americas (Mantilla-Meluk et al. 2009). However,
the bat richness of Colombia is not evenly
distributed across its biogeographic regions.
Differences in energy availability across regions
might be an underlying ecological constraint
(Ruggiero and Kitzberger 2004), but this uneven
distribution of bat richness also reflects that some
areas have been better sampled than others, thus
producing patterns that are biased due to
differences in sampling effort. For example,
Stevenson et al. (2004) and Mantilla-Meluk et al.
(2009) have shown that the number of
publications and sampling sites for bats are
clumped in the Andes and strongly biased towards
areas adjacent to the three largest cities in
Colombia: Bogotá, Cali, and Medellín. A larger
number of bat species lists and other peer-
reviewed publications came from departments
within the Andes (e.g., Castaño et al. 2003;
Estrada-Villegas et al. 2010) than from other
biogeographic regions (Marín-Vásquez and
Aguilar-González 2005). One of these
undersampled biogeographic regions is Orinoquía
(Stevenson et al. 2004).
Orinoquía, defined by the Orinoco River
Basin, is located on the eastern versant of the
Andes and is composed of lowland savannas and
Andean ecosystems. It comprises approximately
20.2% (17.4 million ha) of Colombia’s total area,
and four of the 11 largest rivers in the country
flow through this region (Arango et al. 2003;
Romero et al. 2004). Orinoquía includes 11
departments, either partially or totally. Casanare is
one of the four departments totally circumscribed
in this region and provides great revenues in terms
of oil and gas production, cattle farming, and palm
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
2
oil production. It is also one of the most degraded
departments in the country, despite its size; 33.9%
of its area has been transformed (Romero et al.
2004), and only three of its 14 natural ecosystems
have more than 10% of their area protected by the
national park system (Arango et al. 2003). In
terms of biodiversity, bats have not been well
studied in Casanare. Apart from a recent species
list (Trujillo et al. 2011) and a detailed study from
one location (Rodríguez 2009), the available
information is scarce, has not been formally
published in the peer-reviewed literature, and
usually relies on data collected in departments
around Casanare. No study has been published yet
performing assemblage analysis or comparing
different sites in Casanare.
The Asociación de Becarios de Casanare
(ABC), a non-profit organization, is carrying out
the largest environmental educational program in
the department up to date and has done detailed
biodiversity assessments in several sites across the
Andean foothills of Casanare and its savannas.
Here we present the results of these assessments,
which represent the first assemblage analysis of
the bats of Casanare. With the information at hand
we asked: (1) how complete were our surveys in
terms of species richness and true diversity? And
(2) what are the diversity patters that emerge from
our surveys and what are the most plausible
explanations for them?
Materials and Methods
The department of Casanare comprises 3.9%
of Colombia’s total area. It is located on the
eastern versant of Cordillera Oriental and bordered
by the departments of Arauca on the north, Meta
on the south, Vichada and Meta on the east, and
Boyacá on the west (Figure 1). According to
Romero et al. (2004), Casanare has eight biomes,
and the amphibiome Arauca-Casanare is the most
common. Annual rainfall varies from 1,500 to
4,500 mm from northeast to southwest, January is
the driest month, and June the rainiest (Aguirre-
Gutiérrez 1999). Altitude varies from 100 to 3,800
m a.s.l., with an average of 350 m a.s.l. (Aguirre-
Gutiérrez 1999).
We carried out seven biodiversity assessments
in different sites, plus occasional non-standardized
samplings in semirural areas in three
municipalities. Sampling was performed in three
out of eight biomes: zonobiome of the humid
tropical foothills Arauca-Casanare, amphibiome
Arauca-Casanare, and helobiome Orinoquian-
Amazonian. The assessments encompass an
altitudinal range of about 1,000 m, sampling a
drastic change in forest structure, landscape
orography, and levels of anthropogenic
transformation (Table 1).
Table. 1. Sampling sites of biodiversity assessments carried out in Casanare, Colombia. Geographic coordinates and
sampling effort for each site are provided.
Sites
Id
Average
elevation
(m)
Season
Coordinates
Net
meters
(m2)
No. of
nights
No. of
hours
Tinije
TIN
191
Both
4º53’42” N
72º24’12” W
270
21
138
Buenos Aires
BUA
369
Dry
4°59'21" N
72°43'2" W
300
7
28
EPF Floreña
EPF
570
Wet
5°26'33" N
72°27'21" W
270
3
12
Volcán blanco
VOB
657
Wet
5°19'47" N
72°33'6" W
105
3
22
Floreña I
FLI
672
Dry
5°29'46" N
72°23'45" W
270
3
12
Pauto J
PAJ
924
Dry
5°23'12" N
72°28'51" W
270
3
16
Pauto M
PAM
1036
Wet
5°24'23" N
72°28'22" W
240
3
12.5
Figure 1. Map of the department of Casanare. 1.
Municipality of Yopal; 2. Municipality of Aguazul; 3.
Municipality of Tauramena; 4. Municipality of Maní; 5.
Municipality of Chámeza. Inset: political map of
Colombia, Orinoco basin (departments of Meta,
Vichada, and Arauca) in gray, department of Casanare
in dark gray.
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
3
Site description
Tinije (TIN) is a wetland with a lake of 179 ha,
surrounded by a matrix of primary and secondary
forests and savannas that become seasonally
flooded. It is shared by the municipalities of
Aguazul and Maní, and a detailed study, focused
not only on bats, but also on other taxonomic
groups, was carried out by Ramírez (2009) and is
available upon request. Sampling effort was
highest at this site (Table 1) and was performed on
savannas adjacent to transitional forests and within
the primary forest that surrounds the lake. The
most abundant plant species found were Protium
sp. Burm.f., Mauritia flexuosa L.f., Licania
subarachnophylla Cuatrec., Mabea occidentalis
Benth., Siparuna quianenesis Aubl., Henriettella
silvestris Gleason., and Davilla nitida (Vahl)
Kubitzki.
Buenos Aires (BUA) is a tract of secondary
forest (55 ha) that surrounds an oil facility and
belongs to Equión Energy, an oil company that
operates in this region of the country. It has been
in an undisturbed forest recovery since 2000.
There are remnants of old gallery forests and
abandoned pastures that have turned into
secondary forests. The most abundant plant
species found there were Genipa americana L.,
Banara guianensis Aubl., Miconia minutiflora
(Bonpl.) DC., and Siparuna guianensis Aubl.
Since 2000 Equión Energy has been actively
protecting this area by banning logging and
hunting.
EPF Floreña (EPF) is an oil processing facility
imbedded in a pasture-secondary-gallery-forest
matrix. We know no actions promoting forest
conservation in the area.
Volcán Blanco (VOB) is a small watershed
with a gallery forest surrounded by pastures.
Forests are secondary in nature but interconnected
with other forest tracts at lower and higher
elevations. The most common tree species found
were Miconia dolichorrhyncha Naudin., Inga
edulis Mart., Ficus insipida Willd., Aniba sp.
Aubl., and Oyedaea verbesinoides DC. This site
had the smallest sampling effort (Table 1) and
there haven’t been any actions promoting forest
conservation in the area that we know of.
Floreña I (FLI) is an area characterized by
well-preserved gallery forests and grasslands for
cattle farming. A particularity of this site is the
abundance of the palm Scheelea sp. in the
grasslands due to the fact that cattle feed on its
fruits. We are not aware of any actions promoting
forest conservation in this area.
Pauto J (PAJ) is an area with very small
remnants of gallery forests imbedded in open
grasslands with very few standing trees. There are
no current conservation efforts in this area. Pauto
M (PAM), despite being very close to Pauto J, has
large fragments of secondary and gallery forests
with small grasslands. Forests were preserved in
this area for unknown reasons until Equión Energy
bought those areas and protected them by banning
logging and hunting since 2009. In general, sites
are distributed along the rainfall gradient present
in Casanare and the aforementioned sites vary in
annual rainfall from 4,500 to 3,000 mm, a
considerable decrease of 1,500 mm of annual
rainfall.
Sampling methods
At each site we conducted mist netting from
18:00 till midnight and from 3:00 till 6:00,
because previous studies in the area demonstrated
that bat activity is extremely low between 0:00
and 3:00. Rainy nights were avoided. Buenos
Aires and Pauto J were sampled in the dry season,
whereas EPF Floreña, Volcán Blanco, Floreña I
and Pauto M were sampled in the rainy season.
Tinije was sampled in both seasons. A preliminary
analysis showed that seasonality did not affect the
differences in relative abundances between sites
(T-TEST, t 5.746= 0.0304 P = 0.9768).
We captured bats with mist nets of different
lengths (6 and 12 m long x 2.5 m high) set up
opportunistically on forest edges, over creeks,
across trails, and inside dense vegetation, in order
to maximize the number of captures and increase
the probability of capturing species that prefer
different habitats. The sampling effort per site was
calculated using a modification of the index
proposed by Straube and Bianconi (2002); square
meters (transforming all nets into 12 m nets)
multiplied by sampling hours. This approach helps
compare sites that were more intensively sampled
than others. Although we tried to avoid nights of
full moon, some sites were sampled close to full
moon due to logistical constraints. Although lunar
phobia is known for some bat species (Morrison
1978), sampling nights near full moon carried out
in places with dense vegetation were as successful
as sampling nights in waning or waxing moon
(Estrada-Villegas and Ramírez personal
observations), so we are confident that capture
success was not strongly affected by moon phase.
All bats that were captured were aged, sexed,
weighed, and measured following standardized
protocols and observing the guidelines of the
American Society of Mammalogists (Sikes and
Gannon 2011). Field identifications and posterior
photographic confirmations were based on Timm
and LaVal (1998), Gardner (2008), Aguirre et al.
(2009) and Díaz et al. (2011). Taxonomy followed
Simmons (2005) but we opted to use Dermanura
for lesser Artibeus according to Hoofer et al.
(2008). We collected voucher specimens from
some species to confirm our field identifications
(Colección Teriológica Universidad de Antioquia
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
4
817-822) and followed specific criteria for some
species that are difficult to identify in the field.
We differentiated Anoura geoffroyi from Anoura
luismanueli by size, as A. luismanueli is smaller in
forearm length and body size, and we followed the
geographic distribution proposed by Mantilla-
Meluk and Baker (2005) for A. luismanueli.
Carollia perspicillata was differentiated from
Carollia brevicauda by its larger forearm length,
lighter banding on the back fur, longer tibia, and
forearm, tibia and feet sparsely haired. When
possible, we checked for size differences between
inner and outer lower incisors as suggested by
Timm and LaVal (1998). Dermanura anderseni
was differentiated from Dermanura glauca by its
sparsely haired uropatagium, duller dorsal pelage
and its rostrum tilted up when seen from the side.
When comparing these species in the field, D.
glauca has well-defined and brighter facial stripes
than D. anderseni (Gardner 2008). We grouped
Platyrrhinus helleri with Platyrrhinus
brachycephalus, because they are
indistinguishable and the two accessory cusps on
the anterior margin of the second premolar are
very difficult to see in the field.
Data analysis
We analyzed our data in two ways; first, we
pooled data from all sites in order to have an
assessment of the whole assemblage, and, second,
abundances were standardized by sampling effort
per site allowing us to unravel patterns at the
landscape level (i.e., among sites). To calculate the
estimated richness (Sest) of the whole assemblage
and the inventory completeness of our surveys, we
took two approaches.
First, we calculated the Jackknife 1 richness
estimator, which performs well compared to other
estimators. It is reliable when habitats within the
landscape are heterogeneous, as in our case, and
suits the type of surveys we performed (Burnham
and Overton 1979; Meyer et al. 2011). For this
analysis we used each sampling night per site and
included an additional row for species that have
been caught occasionally (two bat species in the
municipality of Yopal and two in the municipality
of Chámeza). Then we calculated sampling
completeness as a percentage of estimated
richness.
Second, we compared the observed richness
(Sobs) with the number of bats species that have
been recorded for the department of Casanare and
three departments around it, Arauca, Meta and
Vichada, according to the most up-to-date
mammal species list for Colombia (Solari et al.
2013). Given that the number of studies on bats in
Casanare is low, and these three departments share
the same biomes found in Casanare, probably the
bats present in these three departments are also
present in Casanare. This approach gave us an
upper boundary for the expected number of
species according to their distributions and offered
a way to compare the result obtained with the
Jackknife 1 estimator. The Jackknife 1 richness
estimator was calculated in the package vegan 2.0-
2 for R (Oksanen et al. 2011).
Last, we used a qualitative measure of
abundance developed by Gaston (1994), in which
we consider in how many sites a species occurred.
If a species occurred in more than 75% of the
sites, we considered it super-abundant, abundant if
it occurred in more than 50% of the sites, common
between 50% and 25%, and rare if it occurred in
less than 25% of the sites.
We also chose to describe our survey in terms
of true diversities or effective numbers, which are
derived from parametric families of diversity
functions (Tóthmérész 1995). In our work we used
two families, Rényi’s and Hill’s (Hill 1973; Rényi
1961), which are mathematically related to each
other (Tóthmérész 1995), and change according to
the scale parameter α for Rényi’s, and the order q
for Hill’s, respectively (following the terminology
of Tóthmérész 1995 and Jost 2006). This approach
changes the paradigm of how assemblages are
analyzed. Instead of using different diversity
indices (e.g., Shannon or Simpson), it uses species
frequencies and the order, or scale parameter, of
the functions. Assemblages are described not in
terms of entropy but in terms of individual units or
effective number of species that are biologically
meaningful and comparable.
Effective numbers can be determined as
diversity of order zero, one, two, and infinity (0D,
1D, 2D, and ∞D for Hill numbers or H0, H1, H2 and
H∞ for Rényi diversities). When q or α=0, or
diversity of order zero, the functions are
insensitive to species frequencies and the value
corresponds to the species richness. When q or
α<1, true diversities favors rare species but when
q or α = 1 all species are weighted equally and
only by their frequencies. When q or α > 1 true
diversities favors common species (Jost 2006).
The common diversity indices used in community
ecology are in fact special cases of Hill numbers
or Rényi diversities. For Hill numbers 0D = S, 1D
= exp(H′), 2D = D2, and ∞D = 1/(max pi); for
Rényi diversities H0 = log(S), H1 = H′, H2 = −
log(Σpi2), and H∞ = − log(max pi) for Rényi
diversities (Oksanen et al. 2011). S = species
richness, H’ = Shannon–Weaver index, D2 =
inverse Simpson index and pi = frequency of the
ith species. Both 1/(max pi) and − log(max pi) are
directly related to the Berger-Parker diversity
index d-1 (Kindt et al. 2006).
To analyze the diversity completeness for the
whole assemblage, we calculated 0D, 1D and 2D as
proposed by Moreno et al. (2011) using the
software SPADE (Chao and Shen 2010), and
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
5
calculated the Abundance-based Coverage
Estimator ACE, the Jackknife richness estimator
and the Minimum Variance Unbiased Estimator
MVUE as expected diversities for 0D, 1D and 2D,
respectively. Observed true diversities were
calculated using the Rényi function with the
package vegan 2.0-2 for R and setting the output
for Hill numbers instead of Rényi diversities
(Oksanen et al. 2011).
To compare our sampling sites in order to
detect patterns across the landscape, we ordered
their true diversities calculating a Rényi plot,
which is a reliable method to compare
simultaneously the diversity functions of different
assemblages and determine which one is truly
more diverse (Kindt et al. 2006; Tóthmérész
1995). For this analysis, we corrected species
abundances by dividing abundance per species per
site by the sampling effort employed in that site.
This correction allowed us to account for
differences in sampling effort between
assessments.
Then we calculated the dissimilarity in species
composition between all sampling sites with the
binary version of Horn’s similarity index and used
two-dimensional non-metric multidimensional
scaling (NMDS) to compare assemblage
composition among sites. Horn’s index is a
suitable metric for our study because we are
interested in finding patterns in terms of the
presence/absence data and it is unaffected by small
sample sizes (Krebs 1999). The Rényi plot
complements this pattern elucidation by using
corrected abundance data. Finally, to determine if
there has been an effect of conservation status, we
employed an analysis of similarity (ANOSIM)
based on the dissimilarity matrix used in the
NMDS, and grouped sites by management regime.
For analyzing the effect of elevation on
community composition, we regressed the NMDS
axis 1 against elevation. To calculate the Rényi
profile, the dissimilarity matrix, and the NMDS,
we used the package vegan 2.0-2 for R (Oksanen
et al. 2011). Rényi diversity plots were calculated
using the renyiplot function for R with the
package BiodiversityR version 1.6 (Kindt and Coe
2005). All analyses were performed using R
version 2.14.2 (R Foundation for Statistical
Computing (2012)) except where stated otherwise.
Results
We captured 1,116 individual bats of 51
species and five families in Casanare (Table 2 and
3), including occasional observations.
Phyllostomidae was the richest family, with 39
species, and Stenodermatinae, followed by
Phyllostominae, were the richest subfamilies. We
recorded elusive species in our assessments and
occasional captures, such as Peropteryx macrotis,
Lampronycteris brachyotis, Tonatia bidens,
Sphaeronycteris toxophyllum, Histiotus montanus,
and Lasiurus blossevillii. Six species, including
Desmodus rotundus and Carollia perspicillata,
were super-abundant, four were abundant, 16 were
common, and 23 were rare (Table 2). The
completeness of our surveys was intermediate
(Table 4); the lower boundary, determined by the
richness estimator, showed high completeness
(80.04%). However if we use the expected number
of species according to the species that could be
present in Casanare, Arauca, Meta, and Vichada
(Solari et al. 2013), the completeness of our
surveys was low (51.52%). In terms of true
diversity, the estimated 1D and 2D determined that
the assemblage should have had 1.03 and 0.99
times more effective species, respectively, than
what we were able to record (Table 4).
Figure 3. Non-metric multidimensional scaling (NMDS)
based on the Horn dissimilarity index for seven
sampling sites in Casanare, Colombia. For site
abbreviation please see Table 1.
Figure 2. Rényi diversity profiles for seven sampling
sites in Casanare, Colombia. Occasional observations
were not included in this analysis.
−0.4 −0.3 −0.2 −0.1 0.0 0.1 0.2 0.3
−0.3 −0.2 −0.1 0.0 0.1 0.2 0.3
NMDS1
NMDS2
●
●
●
BUA
EPF
FLI
PAJ
PAM
TIN
VOB
0 0.25 0.5 1 16 2 32 4 64 8 Inf
0 5 10 15 20 25
alpha
H−alpha
Tinije
Buenos Aires
EPF Floreña
Volcán blanco
Floreña I
Pauto J
Pauto M
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
6
Table 2. Bat species list of Casanare, Colombia. Information based on captures made in seven sampling sites.
Family
Subfamily
Species
Qualitative abundance
Emballonuridae
Peropteryx macrotis
1
Saccopteryx leptura
R
Rhynchonycteris naso
R
Noctilionidae
Noctilio leporinus
R
Phyllostomidae
Desmodontinae
Desmodus rotundus
SA
Glossophaginae
Anoura geoffroyi
C
Anoura luismanueli
R
Glossophaga soricina
SA
Lonchophylla sp.
R
Phyllostominae
Lampronycteris brachyotis
R
Lophostoma brasiliense
C
Lophostoma silvicolum
R
Macrophyllum macrophyllum
R
Micronycteris microtis
R
Micronycteris schmidtorum
R
Mimon crenulatum
R
Phyllostomus discolor
C
Phyllostomus elongatus
C
Phyllostomus hastatus
C
Tonatia bidens
R
Tonatia saurophila
R
Trachops cirrhosus
C
Carollinae
Carollia brevicauda
SA
Carollia castanea
C
Carollia perspicillata
SA
Stenodermatinae
Artibeus lituratus
SA
Artibeus obscurus
C
Artibeus planirostris
A
Chiroderma trinitatum
C
Chiroderma villosum
C
Dermanura anderseni
A
Dermanura glauca
C
Mesophylla macconnelli
C
Platyrrhinus
helleri/brachycephalus
SA
Platyrrhinus nigellus
2
Sphaeronycteris toxophyllum
R
Sturnira erythromos
R
Sturnira lillium
C
Sturnira oporaphilum
R
Uroderma bilobatum
A
Uroderma magnirostrum
R
Vampyriscus bidens
R
Vampyressa thyone
A
Vespertilionidae
Myotinae
Myotis albescens
C
Myotis keaysi
R
Myotis nigricans
R
Vespertilioninae
Eptesicus brasiliensis
C
Eptesicus furinalis
C
Histiotus montanus
2
Lasiurus blossevillii
R
Molossidae
Molossus molossus
1
1 Occasional observations made on mist netting nights in the municipality of Yopal.
2 Occasional observations made on netting nights in the municipality of Chámeza. These observations were not
included in our biodiversity assessments; however, these species were included in a separate row to calculate
the estimated richness for all our surveys.
!
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
7
Table 3. Bat species abundance at each sampling site in Casanare, Colombia. For site abbreviations see Table 1.
Species
TIN
BUA
EPF
VOB
FLI
PAJ
PAM
Total
Anoura geoffroyi
0
0
0
1
4
0
0
5
Anoura luismanueli
0
0
0
0
0
0
3
3
Artibeus lituratus
12
1
5
3
3
1
0
25
Artibeus obscurus
7
0
5
0
9
0
0
21
Artibeus planirostris
21
6
0
8
2
9
0
46
Carollia brevicauda
28
5
18
47
18
8
26
150
Carollia castanea
0
12
20
0
0
1
0
33
Carollia perspicillata
143
59
0
4
4
4
6
220
Chiroderma trinitatum
4
0
0
0
0
0
2
6
Chiroderma villosum
0
0
0
0
1
1
0
2
Dermanura anderseni
0
3
1
2
1
0
1
8
Dermanura glauca
6
0
0
0
1
2
0
9
Desmodus rotundus
248
13
2
6
2
4
6
281
Eptesicus brasiliensis
5
1
0
0
0
0
0
6
Eptesicus furinalis
0
0
0
1
0
0
1
2
Glossophaga soricina
3
16
7
6
3
1
0
36
Lampronycteris brachyotis
0
0
0
1
0
0
0
1
Lasiurus blossevillii
2
0
0
0
0
0
0
2
Lophostoma brasiliense
6
1
0
1
0
0
0
8
Lophostoma silvicolum
6
0
0
0
0
0
0
6
Lonchophylla sp.
0
1
0
0
0
0
0
1
Macrophyllum macrophyllum
1
0
0
0
0
0
0
1
Mesophylla macconnelli
2
7
0
0
0
0
1
10
Micronycteris microtis
2
0
0
0
0
0
0
2
Micronycteris schmidtorum
0
4
0
0
0
0
0
4
Mimon crenulatum
25
0
0
0
0
0
0
25
Myotis keaysi
0
0
1
0
0
0
0
1
Myotis nigricans
0
0
0
0
0
1
0
1
Noctilio leporinus
1
0
0
0
0
0
0
1
Phyllostomus discolor
2
3
0
0
0
0
0
5
Phyllostomus elongatus
18
11
0
0
0
0
0
29
Phyllostomus hastatus
2
5
0
0
0
0
0
7
Platyrrhinus helleri/brachycephalus
16
2
10
6
10
2
4
50
Rhynchonycteris naso
12
0
0
0
0
0
0
12
Saccopteryx leptura
2
0
0
0
0
0
0
2
Sphaeronycteris toxophyllum
0
0
1
0
0
0
0
1
Sturnira erythromos
0
0
0
0
1
0
0
1
Sturnira lillium
0
0
0
0
6
0
1
7
Sturnira oporaphilum
0
0
0
0
2
0
0
2
Tonatia bidens
2
0
0
0
0
0
0
2
Tonatia saurophila
0
2
0
0
0
0
0
2
Trachops cirrhosus
17
2
1
0
0
0
0
20
Uroderma bilobatum
0
3
2
2
12
0
1
20
Uroderma magnirostrum
0
21
0
0
0
0
0
21
Vampyriscus bidens
0
3
0
0
0
0
0
3
Vampyressa thyone
0
2
6
1
1
0
2
12
Total abundance
593
184
79
89
80
34
55
1114
Species richness
26
24
13
14
17
11
13
511
1 This tallying includes four occasional observations made in the municipality of Yopal and Chámeza; Peropteryx
macrotis, Platyrrhinus nigellus, Histiotus montanus, and Molossus molossus. Occasional observations are not included in
the tallying of total abundance.
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
8
After correcting for sampling effort, the Rényi
plot showed that no site was truly more diverse
than the others, because the profiles intersect each
other (Figure 2). However, when making closer
comparisons, some patterns emerged. Tinije and
Buenos Aires were more diverse than Pauto M and
Volcán Blanco, and Floreña I was more diverse
than Pauto M, Volcán Blanco, EPF Floreña, and
Pauto J. However, Floreña I overlaps both with
Tinije and Buenos Aires, thus it is not more
diverse than these two sites. At H0, Tinije showed
higher true diversity (i.e., richness) than Buenos
Aires, but Buenos Aires has a more even
assemblage than Tinije given that Tinije’s profile
was steeper than Buenos Aires’s. At H1, Buenos
Aires was 2.02 times more diverse than Volcán
Blanco, the lowest diversity at this scale
parameter, and 1.59 times more diverse than
Tinije, which was more diverse than Buenos Aires
at H0. At H2 and H∞, Floreña I had higher true
diversities than the other sites, which is due to the
fact that Rényi diversities at these scale parameter
favors common species. For example, the most
abundant species in Floreña I had only 22.5% of
the total abundance, whereas the most abundant
species Pauto M and Volcán Blanco had 47.3%
and 52.8% of the total abundance, respectively.
In terms of species composition, the two-
dimensional NMDS had high goodness of fit (R2 =
0.98) and low stress (stress = 0.05), indicating a
high match between the dissimilarity matrix and
the ordination. The NMDS axis 1 (Figure 3)
showed a week environmental gradient in species
composition defined by altitude and a distribution
of sites in the southwest-northeast direction.
Assessments performed at lower altitudes and
towards the southwest seemed to have low scores
along axis 1, whereas assessments at higher
altitudes and towards the northeast seemed to have
higher scores. Nevertheless, axis 2 reflected a
stronger gradient in species composition related to
conservation status; sites surrounded by preserved
forests (Tinije, Buenos Aires and Pauto M) had
high scores along this axis, whereas assessments
performed in unprotected areas (Volcán Blanco,
Floreña I, EPF Floreña and Pauto J) had low
scores. The conservation status of the areas
affected the assemblage structure; species
composition differed significantly between
protected and unprotected areas (ANOSIM, global
R = 0.528, P = 0.026). Although the relationship
between the axis of species composition and
elevation was not significant (T-TEST, F5 = 3.262,
P = 0.131, R2 = 0.274), there seems to be a trend
between elevation and composition (Figure 4).
Discussion
Our study provided the first bat species list and
analysis of assemblage structure and species
composition for the department of Casanare,
Colombia. We found 51 bat species of five
families, which were sampled across
representative biomes of the Orinoco Basin. We
were able to survey both middle-sized and small-
sized forests, allowing us to detect rare species
that usually go unnoticed in inventories carried out
on other Neotropical areas. This work, as far as we
know, its the first study that employed Rényi plots
and true diversities to describe a bat assemblage in
Colombia and one of the few in the Neotropics
(see Moreno et al. 2011 for another example).
Other studies that made preliminary lists of the
bats of Casanare, such as those by Biocolombia
(1996), Vega-Orduz (2007), Garavito-Fonesca
(2008), and Trujillo et al. (2011), have relied
mostly on secondary sources and provided lists
that included species that are not or should not be
present in Casanare according to well-established
distributions. For example, Trujillo et al. (2011)
included Centurio senex and Rhinophylla fisherae,
as well as other species, in their bat list of
Casanare. The former is known to occur only in
the Caribbean coast of Colombia and the latter is
restricted to the Amazon. Thus, their account for
the number of species in the department (112)
might be overestimated. Similarly, Vega-Orduz
(2007) included Rhogeessa minutilla and
Molossus tropidorhynchus in her list: the former is
restricted to dry areas of the northeastern tip of
Colombia and the latter is a subspecies found only
in Cuba and the Cayman Islands. Thus, her list is
also questionable. On her account, Garavito-
Fonesca (2008) used secondary information and
expert advice in order to classify each bat species
as present or likely to be present in the department
and was stated as such in her work. Surprisingly,
Trujillo’s list only differs by two species
compared to Garavito-Fonesca’s, and whereas
Figure 4. Non-metric multidimensional scaling (NMDS)
axis 1 regressed against elevation. For site-specific
elevation, please see Table 1.
200 400 600 800 1000
−0.4 −0.2 0.0 0.2
Elevation
NMDS axis 1
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
9
Garavito-Fonesca clearly states which species are
likely to be present, Trujillo et al. (2011) does not
make such distinction. This casts more doubt on
the list published by Trujillo et al. (2011), which is
the last list published to date. Finally, these
studies, among others, have cited the list published
by Biocolombia (1996) as the most complete list
of the bats present in Casanare. However, this is a
hypothetical list, as the authors in its legend state
it, and authors citing this list have created
confusion because they have used it for purposes
beyond its original intention.
According to our results and the estimated
richness based on possible occurrences (Solari et
al. 2013), the number of bat species present in
Casanare might be between 64 and 99, which is
highly likely because our sampling was biased
towards phyllostomids, excluding emballonurids,
vespertilionids, and molossids (Kalko et al.
2008). In this regard, a recent study on the
watershed of the Pauto River on the Municipalities
of Pore, Trinidad and San Luis de Palenque
(Suárez-Castro et al. 2013), reports three
additional species that we missed in our surveys:
Saccopteryx bilineata, Myotis riparius
and Rhogeessa io. All emballonurids that are
occasionally captured with mist nets. Moreover,
veterinarians from Instituto Colombiano
Agropecuario ICA have caught Diaemus yungi
and Diphylla ecaudata (Tabares, personal
communication), indicating that the number of bat
species in Casanare should be indeed higher than
64, but probably not 112. Sánchez-Palomino et al.
(1993), Muñoz-Saba et al. (1997), and Rojas et al.
(2004) reported similar bat assemblages, although
less rich than the one we describe here. These
studies were carried out on Serranía de la
Macarena (department of Meta), which is strongly
influenced by Amazonian ecosystems. Thus, it is
not surprising that they were able to find
Rhinophylla fisherae. At a regional scale, the
assemblage in Casanare, and specially Tinije, is
similar to the one reported by Aguirre (2002).
Both sites are seasonally flooded savannas with
gallery forests, grasslands, and anthropogenic
areas.
In terms of assemblage structure, our results
concur with other studies (Rojas et al. 2004;
Sánchez-Palomino et al. 1993). Carollia was the
most abundant genus, followed Artibeus.
Desmodus rotundus is very abundant in sites
where cattle has been intensively raised, such as
Casanare, Meta (Sánchez-Palomino et al. 1993),
and also Llanos de Moxos in Bolivia (Aguirre
2002). Moreover, rare species found elsewhere,
like Vampyriscus bidens, Trinycteris nycefori and
Dermanura anderseni (Aguirre 2002; Rojas et al.
2004; Sánchez-Palomino et al. 1993), were also
rare in our study. Only a few studies have
analyzed assemblages with the true diversity
approach. Moreno et al. (2011) seems to be the
first to encourage its use in analysis of bat
assemblages. Our results suggest that the
estimated true diversities for the whole
assemblage (all sites pooled together) is high and
indicates marked differences between sites that do
not overlap their diversity profiles. These
differences, however, should be interpreted with
caution because sampling effort varied among
sites. This is due to the fact that different
biodiversity assessments aimed at different goals
(e.g., public vs. private contracts), some were
intended to be more intensive than others, and the
time available to perform them also varied. One
pattern, however, is clear: Floreña I has higher
true diversity than EPF Floreña, Volcán Blanco,
Pauto J and Pauto M, all sampled with very
similar efforts.
Species composition seems to reflect the
results in terms of structure. Tinije and Buenos
Aires showed high scores on the NMDS axis 2
and higher diversity profiles than other sites, both
to the southwest of our study area and protected to
some degree. Again, we cannot rule out the effect
of sampling effort but cannot rule out either a
compounded effect of forest preservation and
altitude on species composition. Still, the effect of
forest conservation was evident in terms of
assemblage composition (see ANOSIM) and there
seems to be a changing trend with respect to
altitude. A monotonic decrease in bat richness
with altitude has been found in Peru (Graham
1983; Patterson et al. 1996; Solari et al. 2006) and
Bolivia (Vargas and Patterson 2007), but other
examples from Colombia (Fawcett 1994; Munoz
1990) suggest a mid-elevation peak. However,
Table 4. Observed and estimated true diversities, estimated species richness, and percentage of completeness for
the bat assemblage of Casanare, Colombia. All occasional observations were included in the analysis. Sobs = 51.
Estimator
0D
1D
2D
Sest
Completeness
Observed by SPADE
51
14.204
7.773
Expected by SPADE
62
14.625
7.783
Expected by Jackknife 1
63.72
80.04%
Expected by Solari et al. (2013)
99
51.52%
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
10
Mantilla-Meluk (2009), using museum records for
Phyllostomids at the scale of the whole country,
and Marín-Vásquez and Aguilar-Gonzáles (2004),
in a mountain range on the eastern versant of
Cordillera Oriental, have shown a decreasing
linear trend.
Our results, in part, concur with their findings,
although our range only spans about 1,000 m and
sampling efforts have not been the same across
elevations. Although we did not find a decrease in
richness with elevation, the change in assemblage
composition is somehow evident. The species
richness elevation trend seems to be explained by
poor thermoregulatory capabilities of Neotropical
bats due to their small size and high surface to
volume ratio (Soriano 2000), and not by available
area or the mid-domain effect as it was claimed
before McCain’s work (2007).
Forest conservation is also known to have
paramount consequences on bat assemblage
structure and composition because anthropogenic
transformation reduces the number of rare species
and enhances the abundance of common species
(Ewers and Didham 2006; Meyer and Kalko
2008). In our case, phyllostomines such as
Phyllostomus elongatus, Tonatia saurophila, and
Lophostoma silvicolum, known as indicators of
preserved forests (Meyer and Kalko 2008), were
only found in protected areas. However, how
should we interpret the fact that Floreña I, which
is not protected, showed higher true diversity than
the other sites? We think this is related to habitat
quality at the sampling sites: the size of the stream
and its gallery forest was larger than in other sites
and bats seem to be attracted to this type of area in
the dry season. Finally, species composition in
Casanare also showed a climatic gradient, where
assemblages seemed to change in the southwest-
northeast direction, as suggested by the ordination.
This seems plausible given that rainfall decreases
from southwest to northeast (Aguirre-Gutiérrez
1999), and rainfall is an important structuring
factor of bat assemblages (Estrada-Villegas et al.
2012). Nonetheless, this hypothesis should be
further investigated given that we were unable to
study each site during both climatic seasons and/or
with similar sampling efforts.
In conclusion, we present a species list of the
department of Casanare based on field data and
compare our results with those of previews
studies, most of them based on hypothetical
presences. We show for the first time an
assemblage-level analysis for the bats of Casanare,
and as far as we know, we are the first to use true
diversities and diversity profiles to compare bat
assemblages in Colombia. With these analyses we
show that forest management has a positive effect
on assemblage composition, which also changes
with elevation.
Acknowledgments
Studies in Buenos Aires, Floreña I, Pauto M,
Pauto J, EPF Floreña, and Volcán Blanco were
funded by Equion Energía Limited. We thank all
its external affairs and environmental teams for
the financial and logistic support. The study in
Tinije was co-funded by Gobernación de
Casanare; we thank Manuel Rodríguez for his
hard work and support for this study. Occasional
captures in Chámeza were funded by the
Municipality of Chámeza. We thank our field
assistants and the local communities, as well as
our work team at ABC. We thank S. Solari and M.
Rodríguez-Posada for species identification.
Julieta Garavito deserves special thanks for
sharing her Master’s thesis and data with us.
Finally, we thank Ricardo Tabares from Instituto
Colombiano Agropecuario ICA for information
about other vampire species he has captured.
Research permits were issued by Corporinoquia
(numbers 500.57.12-0451, 200.41-10.1409, and
200.41.09.0681).
References
Aguirre L.F. 2002. Structure of a Neotropical
savanna bat community. Journal of Mammalogy
83(3): 775-784.
Aguirre L.F.; Vargas A. and Solari S. 2009. Clave
de campo para la identificación de los
murciélagos de Bolivia. Centro de Estudios en
Biología Teórica y Aplicada, Cochabamba,
Bolivia.
Aguirre-Gutiérrez N. 1999. Casanare:
caracteríticas geográficas. Instituto Geogáfico
"Agustín Codazzi", Bogotá.
Alberico M. C.A., Hernández-Camacho J., Y.
Muñoz-Saba. 2000. Mamíferos (Synapsida:
Theria) de Colombia. Biota Colombiana 1(1):
43-75.
Arango N.; Armenteras D.; Castro M.; Gottsmann
T.; Hernández O.L.; Matallana C.L.; Morales
M.; Naranjo L.G.; Renjifo L.M.; F. T.A. and
Villareal H.F. 2003. Vacíos de conservación del
sistema de Parques Nacionales Naturales de
Colombia desde una perspectiva ecorregional.
WWF Colombia and Instituto de Investigación
de Recursos Biológicos Alexander von
Humboldt, Bogotá.
Biocolombia. 1996. Faunula de vertebrados y su
entorno en la región de los campos de Cusiana y
Cupiagua -Departamento de Casanare- Bases
para su uso, conservación y manejo. Informe
final. Bogotá
Burnham K.P. and Overton W.S. 1979. Robust
estimation of population size when capture
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
11
probabilities vary among animals. Ecology 60:
927–936.
Castaño J.H.; Muñoz-Saba Y.; Botero J.E. and
Vélez J.H. 2003. Mamíferos del departamento
de Caldas-Colombia. Biota Colombiana 4(2):
247-259.
Chao A. and Shen T.-J. 2010. Program SPADE
(Species prediction and diversity estimation)
http//:chaostatnthuedutw.
Díaz M.M.; Aguirre L.F. and Barquez R.M. 2011.
Clave de identificación de los murciélagos del
cono sur de Sudamérica. Centro de Estudios en
Biología Teórica y Aplicada., Cochabamba,
Bolivia.
Estrada-Villegas S.; McGill B.J. and Kalko E.K.V.
2012. Climate, habitat, and species interactions
at different scales determine the structure of a
Neotropical bat community. Ecology. Doi.
http://dx.doi.org/10.1890/11-0275.1
Estrada-Villegas S.; Pérez-Torres J. and Stevenson
P.R. 2010. Ensamblaje de murciélagos en un
bosque subandino colombiano y análisis sobre
la dieta de algunas especies. Mastozoología
neotropical 17(1): 31-41.
Ewers R.M. and Didham R.K. 2006. Confounding
factors in the detection of species responses to
habitat fragmentation. Biological Reviews
81(1): 117-142.
Fawcett D. 1994. Bats. in Surveys and
conservation of biodiversity in the Chocó,
south-west Colombia (edited by Salaman
P.G.W.), pp. 60-67. BirdLife International,
Cambridge.
Garavito-Fonseca J. 2008. Priorización de áreas
para la conservación de la mastofauna silvestre
en Casanare - Colombia. Masters, Vicerectorado
de Producción Agrícola, Universidad Nacional
Experimental de los Llanos Occidentales
"Ezequiel Zamora".
Gardner A.L. 2008 [2007]. Mammals of South
America, Volumen 1 Marsupials, Xenarthrans,
Shrews, and Bats. The University of Chicago
Press, Chicago.
Gaston K.J. 1994. Rarity. Chapman & Hall,
London.
Graham G.L. 1983. Changes in bat species
diversity along an elevational gradient up the
Peruvian Andes. Journal of Mammalogy 64(4):
559-571.
Hill M.O. 1973. Diversity and evenness: A
unifying notation and its consequences. Ecology
54(2): 427-432.
Hoofer S.R.; Solari S.; Larsen P.A.; Bradley R.D.
and Baker R.J. 2008. Phylogenetics of the fruit-
eating bats (Phyllostomidae: Artibeina) inferred
from mitochondrial DNA sequences. Occasional
Papers, Museum of Texas Tech University 277:
1–15.
Jost L. 2006. Entropy and diversity. Oikos 113(2):
363-375.
Kalko E.K.V.; Estrada-Villegas S.; Schmidt M.;
Wegmann M. and Meyer C.F.J. 2008. Flying
high-assessing the use of the aerosphere by bats.
Integrative and Comparative Biology 48(1): 60-
73.
Kindt R. and Coe R. 2005. Tree diversity analysis:
A manual and software for common statistical
methods for ecological and biodiversity studies.
World Agroforestry Centre (ICRAF), Nairobi.
Kindt R.; Damme P. and Simons A. 2006. Tree
diversity in western Kenya: using profiles to
characterise richness and evenness. Biodiversity
and Conservation 2(15):1253–1270.
Krebs C.J. 1999. Ecological Methodology.
Addison Wesley Longman, Menlo Park,
California.
Mantilla-Meluk H. and Baker R.J. 2005.
Systematics of Small Anoura (Chiroptera:
Phyllostomidae) from Colombia, with
description of a new species. Occasional Papers,
Museum of Texas Tech University (261), 1-18.
Mantilla-Meluk H.; Jiménez-Ortega A.M. and
Baker R.J. 2009. Phyllostomid bats of
Colombia: Annotated checklist, distribution, and
biogeography. Special Publications Museum of
Texas Tech University, Lubbock, TX.
Marín-Vásquez A. and Aguilar-González A.V.
2004. Diversidad de murciélagos en un
gradiente altitudinal en la vertiente oriental de la
cordillera oriental de los andes Colombianos
(Florencia-Caqueta). Undergraduate, Facultad
de Ciencias Básicas Universidad de la
Amazonía.
Marín-Vásquez A. and Aguilar-González A.V.
2005. Murciélagos (Chiroptera) del
departamento de Caquetá-Colombia. Biota
Colombiana 6(2): 211-218.
McCain C.M. 2007. Area and Mammalian
Elevational Diversity. Ecology 88(1): 76-86.
Meyer C.F.J.; Aguiar L.M.S.; Aguirre L.F.;
Baumgarten J.; Clarke F.M.; Cosson J.-F.;
Villegas S.E.; Fahr J.; Faria D.; Furey N.; Henry
M.; Hodgkison R.; Jenkins R.K.B.; Jung K.G.;
Kingston T.; Kunz T.H.; Cristina MacSwiney
Gonzalez M.; Moya I.; Patterson B.D.; Pons J.-
M.; Racey P.A.; Rex K.; Sampaio E.M.; Solari
S.; Stoner K.E.; Voigt C.C.; von Staden D.;
Weise C.D. and Kalko E.K.V. 2011. Accounting
for detectability improves estimates of species
richness in tropical bat surveys. Journal of
Applied Ecology 48(3): 777-787.
Meyer C.F.J. and Kalko E.K.V. 2008.
Assemblage-level responses of phyllostomid
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
12
bats to tropical forest fragmentation: land-bridge
islands as a model system. Journal of
Biogeography 35(9): 1711-1726.
Moreno C.E.; Barragán F.; Pineda E. and Pavón
N.P. 2011. Reanálisis de la diversidad alfa:
alternativas para interpretar y comparar
información sobre comuniades ecológocas.
Revista Mexicana de Biodiversidad 82(1249-
1261).
Morrison D.W. 1978. Lunar phobia in a
neotropical bat, Artibeus jamaicensis
(Chiroptera: Phyllostomidae). Animal
Behaviour 26: 852-855.
Muñoz A.J. 1990. Diversity and feeding behavior
of bats in an altitudinal transect across the
Cordillera Central of the Colombian Andes.
Studies on Neotropical Fauna & Environment
25(1): 1-18.
Muñoz-Saba Y.; Cadena A. and Rangel-Ch, J. O.
1997. Ecología de los murciélagos antófilos del
sector La Curia, Serraína La Macarena
(Colombia). Revista de la Academia
Colombiana de Ciencias 21(81): 473-486.
Oksanen J.F.; Blanchet G.; Kindt R.; Legendre P.;
Minchin P.R.; O'Hara R.B.; Simpson G.L.;
Solymos P.; Stevens M.H.M. and Wagner H.
2011. vegan: Community Ecology Package
version 2.0-2. http://CRAN.R-
project.org/package=vegan.
Patterson B.D.; Pacheco V. and Solari S. 1996.
Distribution of bats along an elevational
gradient in the Andes of Peru. Journal of
Zoology 240(4): 637-658.
R Development Core Team (2012). R: A language
and environment for statistical computing. R
Foundation for Statistical Computing, Vienna,
Austria.
Ramírez B.H. 2009. Establecimiento de la
composición biológica y estructura ecológica de
la laguna que conforma el humedal “Laguna El
Tinije”, que permitan conocer su dinámica,
estructura y funcionalidad tendiente a su
postulación como área Ramsar. Convenio de
Cooperación No. 0126 de 10 de Diciembre de
2008. Dirección Técnica de Medio Ambiente,
Secretaría de Agricultura, Ganadería y Medio
Ambiente, Gobernación de Casanare.
Asociación de Becarios de Casanare. Informe
Técnico Final. . Yopal.
Rényi A. 1961. On measures of entropy and
information. in Proceedings of the 4th Berkeley
Symposium on Mathematical Statistics and
Probability (edited by Neyman J.), pp. 547-561.
University of California Press, Berkeley, United
States of America.
Rodríguez M. 2009. Mastofauna. in
Establecimiento de la composición biológica y
estructura ecológica de la laguna que conforma
el humedal “Laguna El Tinije”, que permitan
conocer su dinámica, estructura y funcionalidad
tendiente a su postulación como área Ramsar
Convenio de Cooperación No 0126 de 10 de
Diciembre de 2008 Dirección Técnica de Medio
Ambiente, Secretaría de Agricultura, Ganadería
y Medio Ambiente, Gobernación de Casanare
(edited by Ramírez B.), pp. 215-237. Asociación
de Becarios de Casanare, Yopal.
Rojas A.M.; Cadena A. and Stevenson P. 2004.
Preliminary study of the bat community at the
CIEM, Tinigua National Park, Colombia. Field
Studies of Fauna and Flora La Macarena,
Colombia 14: 45-53.
Romero M.; Galindo G.; Otero J. and Armenteras
D. 2004. Ecosistemas de la cuenca del Orinoco
colombiano. Bogotá, Colombia.
Ruggiero A. and Kitzberger T. 2004.
Environmental correlates of mammal species
richness in South America: effects of spatial
structure, taxonomy and geographic range.
Ecography 27(4): 401-417.
Sánchez-Palomino P.; Rivas-Pava P. and Cadena
A. 1993. Composición, abundancia y riqueza de
especies de la comunidad de murciélagos en
bosques de galería en la serranía de La
Macarena (Meta-Colombia). Caldasia 17(2):
301-312.
Sikes R.S. and Gannon W.L. 2011. Guidelines of
the American Society of Mammalogists for the
use of wild mammals in research. Journal of
Mammalogy 92(1): 235-253.
Simmons N.B. 2005. Order Chiroptera. in
Mammal species of the world: a taxonomic and
geographic reference (edited by Wilson D.E.
and Reeder D.M.), pp. 312-529. The Johns
Hopkins Press, Baltimore.
Solari, S.; Muñoz-Saba, Y.; Rodríguez-Mahecha,
J.V.; Defler, T.R.; Ramírez-Chaves, H.E. and
Trujillo F. 2013. Riqueza, endemismo y
conservación de los mamíferos de Colombia.
Mastozoología Neotropical 20(2): 301-365.
Solari S.; Pacheco V.; Luna L.; Velazco P.M. and
Patterson B.D. 2006. Mammals of the Manu
Biosphere Reserve. Fieldiana Zoology 110: 13.
Soriano P. 2000. Functional structure of bat
communities in tropical rainforest and andean
cloud forest. Ecotropicos 13 (1): 1-20.
Stevenson P.; Perez J. and Munoz Y. 2004. Estado
del conocimiento sobre los mamíferos terrestres
y voladores de Colombia. in Informe nacional
sobre el avance en el conocimiento y la
información de la biodiversidad 1998-2004
Tomo II (edited by Chaves M.E. and
Santamaría M.), pp. 151-170. Instituto de
Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
!
!
!
13
Investigación de Recursos Biológicos Alexander
von Humboldt, Bogotá D.C.
Straube, F. C. and Bianconi, G. V. 2002. Sobre a
grandeza e a unidade utilizada para estimar
esforço de captura com utilização de redes-de-
neblina. Chiroptera Neotropical, Brasília 8(1-2):
150-152.
Suárez-Castro, A.F.; Bueno-Castellanos J.C. and
Mora--Fernández C. 2013. Mamíferos, in Guía
de campo. Flora y fauna de las sabanas
inundables asociadas a la cuenca del río Pauto,
Casanare--Colombia (edited by Mora-
-Fernández C. and Peñuela--Recio L.), pp. 200-
234. Serie Biodiversidad para la Sociedad No. 3.
Yoluka ONG, fundación de investigación en
biodiversidad y conservación, Fundación
Horizonte Verde and Ecopetrol S.A.
Timm R.M. and LaVal R.K. 1998. A field key to
the bats of Costa Rica. Occasional Publication
Series, University of Kansas 22: 1-30.
Tóthmérész B. 1995. Comparison of different
methods for diversity ordering. Journal of
Vegetation Science 6(2): 283-290.
Trujillo F.; Garavito-Fonseca J.; K. G.; Rodríguez-
Maldonado M.V.; Combariza R.; Solano-Pérez
L.; Pantoja G. and Ávila-Guillen J.P. 2011.
Mamíferos de Casanare. in Biodiversidad de
Casanare: Ecosistémas Estratégicos del
Departamento (edited by Usma J.S. and Trujillo
F.), pp. 286. Gobernación de Casanare-WWF
Colombia, Bogotá.
Vargas A. and Patterson B.D. 2007. Comunidades
de murciélagos montanos en Bolivia. in Historia
natural, distribución y conservación de los
murciélagos de Bolivia (edited by Aguirre L.F.),
pp. 82-86. Editorial Centro de Ecología y
Difusión Simón I. Patiño, Santa Cruz de la
Sierra.
Vega-Orduz L.F. 2007. Mamíferos de Casanare:
Una Aproximación a la riqueza de especies y los
ecosistemas donde habitan. Informe Final.
Yopal.
