2297Sanchezetal2006BatsPatiaChicamocha

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Original investigation
Bat assemblage structure in two dry forests of Colombia:
Composition, species richness, and relative abundance
By F. Sánchez, J. Alvarez, Clara Ariza and A. Cadena
Instituto de Ciencias Naturales and Departamento de Biologı́a and Universidad Nacional de Colombia,
Bogotá, Colombia
Receipt of Ms. 19.11.2005
Acceptance of Ms. 17.8.2006
Abstract
We studied the composition, species richness, and relative abundance of bat assemblages in the
Colombian dry forests of Chicamocha and Patı́a. In Chicamocha, 11 bats of the family
Phyllostomidae were captured with mist-nets, corresponding to 85–100% of the potential
phyllostomids species in the area. Two bats of the family Vespertilionidae were also captured in
Chicamocha. In Patı́a, 12 species were captured with mist-nets, all Phyllostomidae, representing
72–100% of the estimated total number of species in the zone. Minor differences in number of
species and composition were detected among sampling periods in Chicamocha. The most common
species in this dry forest were Glossophaga longirostris and Sturnira lilium. In Patı́a, notable
differences in the number of species and composition were observed among sampling periods, and
the most common species were Artibeus jamaicensis, Carollia perspicillata and Phyllostomus discolor.
Arid-zone dwelling bats were absent in Patı́a and we suggest that this absence may be associated
with the isolation of Patı́a from other northern dry zones of Colombia since Quaternary times. There
was also low abundance of bats in Patı́a, which appears to be related to human disturbance. The
most abundant phyllostomid bat species in the two dry forests studied are those that include fruit
and/or nectar-pollen from columnar cacti as an important proportion of their diets.
r 2006 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Key words: Chiroptera, Colombia, tropical dry forest
Introduction
The tropical dry forest is an intermediate
formation between the tropical savanna and
the tropical humid forest. Dry forests have at
least one period of water deficiency that
imposes a major limitation for vegetation
growth (Gentry 1995). This formation occurs
in tropical and subtropical areas with mean
annual temperature above 17 1C, mean annual rainfall between 250 and 2000 mm, and
the annual ratio of potential evapotranspira-
tion to precipitation exceeding unity (Murphy and Lugo 1986).
Dry tropical forests are less complex floristically and structurally than wet tropical
forests, and generally have smaller and more
thorny species (Murphy and Lugo 1986;
Gentry 1995). In South America, dry forests
constitute about 22% of the forested area
(Murphy and Lugo 1986). The largest areas
of this forest type are located in north-eastern
1616-5047/$ - see front matter r 2006 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
doi:10.1016/j.mambio.2006.08.003
Mamm. biol. ] (]]]]) ] ]]]–]]]
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
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2
F. Sánchez et al.
Brazil (also known as Caatingas) and along
the Caribbean coasts of Colombia and
Venezuela (Sarmiento 1975). In addition,
dry forests are also present in dry enclaves
in the Andes of Colombia, Venezuela,
Ecuador, Peru and Bolivia, on the coasts of
Ecuador and Peru, and in central Brazil
(Sarmiento 1975; Pennington et al. 2000).
Neotropical dry forests have been recognized
as threatened ecosystems (Stotz et al. 1996),
because most of the forest remnants are
located in areas with intensive agricultural
activity (Murphy and Lugo 1986). It has been
estimated that less than 2% of the original
cover of dry forest persists in Colombia
(Etter 1993, cited by Gast et al. 1997).
Therefore, inventories of fauna and flora,
and information on the ecology of animals
and plants inhabiting Colombian dry forests
is crucial for planning and implementing
management and conservation strategies of
this ecosystem (Gast et al. 1997).
Bats can influence the dynamics of Neotropical forests because they disperse seeds and
pollen for many plant taxa, and they are
important predators (van der Pijl 1957;
Fleming 1993; Patterson et al. 2003; Bonato
et al. 2004). For example, in Neotropical arid
and semiarid zones, Glossophaginae bats
may play key roles for the pollination and
seed dispersal of several species of cacti and
agaves (Petit 1995, 1997; Sosa and Soriano
1996; Ruiz et al. 1997; Naranjo et al. 2003;
Nassar et al. 2003). However, little attention
has been paid to bat assemblages in Neotropical dry forests (Fleming et al. 1972;
Stoner 2001). Thus, the aim of this study was
to investigate the species composition, species
richness and relative abundance of bats in
two dry forests of Colombia, the Chicamocha
River Valley and Patı́a River Valley.
Material and methods
Study sites
The study was conducted at the Chicamocha and
Patı́a river valleys. The subxerophytic character of
these transverse inter-Andean valleys is produced
by the rain-shadow effect of the surrounding
mountains (Hernández-Camacho et al. 1995). In
these two areas, xerophytic scrub is the dominant
physiognomic type, although certain distinctive
forest elements occur at the borders of rivers and
gulches.
The Chicamocha region is located in the northeastern part of the country on the western slope of
the Eastern Cordillera (Fig. 1), in the middle part
of the Chicamocha river basin (Department of
Santander, 61490 N; 731000 W). Its average annual
temperature is 25.4 1C, with average relative
humidity of 65%. The average annual precipitation
is 730.7 mm, and its distribution follows a bimodaltetraseasonal pattern with two pluviosity peaks: the
first between April and May, and the second
between September and October. The shrub Lippia
origanoides, the tree Prosopis juliflora and the
columnar cactus Stenocereus griseus are abundant
in the zone (Albesiano et al. 2003).
The Patı́a region is located in the southwest of
Colombia between the Western and Central
Cordilleras (Fig. 1), in the upper Patı́a river basin
(Department of Nariño, 11 430 N; 771190 W). The
average annual temperature is 25.21C, and the
average relative humidity is 79%. The annual
average precipitation is 809.3 mm distributed in a
bimodal-tetraseasonal pattern. Rainfall is concentrated between March and May, and between
October and December. In this zone, the shrubs
L. origanoides, Lantana canescens and Senna
pallida, and the cacti S. griseus, Pilosocereus sp.
and Opuntia dillenii are abundant.
Sampling
In Chicamocha, sampling was carried out in
October and December of 1995, and in February,
April and July of 1996, at sites located between 500
and 600 m of altitude. In Patı́a, samplings took
place in October and December 1996, and in
February, April, June and September of 1997, at
sites located between 500 and 900 m of altitude.
Four to six mist-nets (9 m 2 m) were set on nights
of low moon brightness, between 19:00 h and
23:00 h (Tab. 1). Independent mist-nets, separated
50–100 m from each other, were set at heights
ranging from 0.2 to 3.0 m above the ground. In
both areas, the captures were performed in thorny
dry scrub, riparian forests, and disturbed (human
or cultivated) areas. Nets were always placed in a
different place at each capture site. We marked bats
with numbered aluminum bands or tattoos made
with a tattoo set for rabbits. The bands were placed
on the forearm, and we only used them in the first
two samplings in Chicamocha because some bats
(e.g., Artibeus spp.) chew the bands. During the rest
of the sampling periods, we used tattoos placed on
the plagiopatagium, because they provided a
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
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Bats of two tropical dry forests of Colombia
3
Fig. 1. Location of the Colombian semiarid zones of the Chicamocha River (1), Patı́a River (2), upper Cauca River
(3), Tatacoa (4), Lagunillas (5), north of Colombia (6), and north of Venezuela (7); and the tentative location of
the humid barrier (8) that separated the Caribbean arid zones and those along the Cauca River Valley during the
Pleistocene according to Hernández-Camacho et al. (1992).
permanent mark. Bats were released after identification to species level. From each species, one to
four adult individuals, half male and half females
when possible, were collected as voucher specimens, and were subsequently deposited in the
mammal collection of the Instituto de Ciencias
Naturales (ICN), Universidad Nacional de Colombia. Identifications in the field were done using the
keys of Linares (1987) and Vizotto and Taddei
(1973). Identification of voucher specimens was
done using literature specific for every family or
genus, and by comparison with museum specimens
from the ICN.
Species richness
We used individual-based rarefaction curves to
compare species richness between the two study
sites (Colwell et al. 2004). As pointed out by
Simmons and Voss (1998), individual-based rather
than sample-based curves are preferred when using
mist-nets to capture bats, because each captured
bat is equally informative about local diversity. We
also used the non-parametric estimators of Chao 1,
Chao 2, incidence-based coverage (ICE), abundance-based coverage (ACE), and first and second
Jackknife (reviewed by Colwell and Coddington
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
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F. Sánchez et al.
Table 1. Sampling effort and bat relative abundance during sampling periods in the Chicamocha region between
October 1995 and July 1996 (A), and in the Patı́a region, between October 1996 and September 1997 (B).
A. Chicamocha
Oct–95
Dec–95
Feb–96
Apr–96
Jul–96
Total
Total nets
Total hours
Total nights
Captured individuals
Capture effort (net. hour)
Relative abundance (bats (net. hour)1)
24
27
6
116
648
0.18
28
31.5
7
113
882
0.13
32
32
8
64
1024
0.06
35
28
7
102
980
0.10
35
38
7
114
1330
0.09
154
156.5
35
509
4864
0.11
B. Patı́a
Oct–96
Dec–96
Feb–97
Apr–97
Jun–97
Sep–97
Total
Total nets
Total hours
Total nights
Captured individuals
Capture effort (net. hour)
Relative abundance (bats (net. hour)1)
30
25
7
16
750
0.02
30
25
7
18
750
0.02
30
25
7
56
750
0.08
35
25
7
78
875
0.09
30
25
7
30
750
0.04
35
25
7
46
875
0.05
190
150
42
244
4750
0.05
1994) to estimate total species richness. Rarefaction
curves and the species richness estimators (after
randomizing the samples 100 times) were obtained
using EstimateS 7.5 (Colwell 2005). Since mist-nets
are not suitable for unbiased sampling of aerial
insectivorous bats (Fleming et al. 1972; Kalko et al.
1996), we only included phyllostomid bats in the
analysis of species richness.
caught by hand in both sites. The species list
of Chicamocha can be complemented with
two species that have been previously captured in this region, Natalus tumidirostris and
Mormoops megalophylla (ICN specimens
5002–5003, 5542–5550 and 5576–5594, respectively).
Species relative abundance
Species richness
We expressed bat abundance relative to the capture
effort in every sampling period (Tab. 1). Effort was
calculated as the product of the number of nets
times number of hours sampled. Recaptured
individuals and bats captured with methods other
than mist-nets were not included in the calculations
of abundance. Given that we had only five samples
from Chicamocha and six from Patı́a, we compared
the relative abundance of phyllostomid bats in the
two sites using the Mann–Whitney test (Zar 1999).
Results
Species composition
In Chicamocha, we captured 13 species of the
Phyllostomidae and Vespertilionidae families
(Tab. 2) with mist-nets. In Patı́a, we captured
12 Phyllostomidae using the same method
(Tab. 3). One individual of the family
Emballonuridae, Peropterix macrotis, was
The rarefaction curve for the Phyllostomidae
in Chicamocha almost reached a plateau,
whereas that for Patı́a did not (Fig. 2). At 210
individuals there were more expected species
in Patı́a (12) than in Chicamocha (10), but
this difference was not significant (Mao Tau
estimator Po0.05, Fig. 2). Nevertheless, the
estimators of total species richness indicated
that Patı́a potentially had a higher richness of
Phyllostomidae than Chicamocha (Tab. 4).
These estimators also suggested that between
85–100% and 72–100% of the potential
phyllostomids were captured in Chicamocha
and Patı́a, respectively.
In the Chicamocha region, the number of
species found in different sampling periods
had minor variations, and five Phyllostomidae (Artibeus jamaicensis, Artibeus lituratus,
Carollia perspicillata, Glossophaga longirostris, Sturnira lilium) and one Vespertilionidae
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
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Bats of two tropical dry forests of Colombia
5
Table 2. Bats captured at the Chicamocha region using mist-nets, between October 1995 and July 1996. N:
number of individuals. RA: relative abundance, bats (net. hour)1.
Species
Oct–95
Phyllostomidae
Sturnira lilium
Glossophaga longirostris
Artibeus lituratus
Artibeus jamaicensis
Glossophaga soricina
Carollia perspicillata
Leptonycteris curasoae
Phyllostomus discolor
Micronycteris megalotis
Carollia brevicauda
Desmodus rotundus
Vespertilionidae
Rhogeessa io
Lasiurus borealis
Dec–95
Feb–96
Apr–96
Jul–96
Total
N1
RA1
N2
RA2
N3
RA3
N4
RA4
N5
RA5
NT
RAT
31
43
1
4
21
1
2
1
5
1
0
.048
.066
.002
.006
.032
.002
.003
.002
.008
.002
0
41
22
19
5
5
6
9
2
1
0
0
.047
.025
.026
.006
.006
.007
.010
.002
.001
0
0
15
23
7
2
3
4
4
0
0
0
0
.015
.023
.007
.002
.003
.004
.004
0
0
0
0
40
11
16
13
0
3
0
6
1
0
0
.041
.011
.016
.013
0
.003
0
.006
.001
0
0
27
41
16
13
0
4
0
4
0
4
1
.020
.031
.012
.010
0
.003
0
.003
0
.003
.001
154
140
59
37
29
18
15
13
7
5
1
.032
.029
.012
.008
.006
.004
.003
.003
.001
.001
.0002
6
0
.009
0
3
0
.003
0
6
0
.006
0
11
1
.011
.001
4
0
.003
0
30
1
.006
.0002
Table 3. Bats captured in the Patı́a region using mist-nets, between October 1996 and September 1997. N:
number of individuals. RA: relative abundance, bats (net. hour)1.
Species
Phyllostomidae
Artibeus jamaicensis
Carollia perspicillata
Phyllostomus discolor
Anoura geoffroyi
Micronycteris megalotis
Choeronycteris godmani
Desmodus rotundus
Sturnira erythromos
Sturnira lilium
Artibeus hartii
Phyllostomus hastatus
Chiroderma salvini
Oct–96
Dec–96
Feb–97
Apr–97
Jun–97
Sep–97
Total
N1
RA1
N2
RA2
N3
RA3
N4
RA4
N5
RA5
N6
RA6
NT
RAT
8
3
2
0
0
0
1
0
0
1
0
1
.011
.004
.003
0
0
0
.001
0
0
.001
0
.001
4
3
2
6
0
2
0
0
0
1
0
0
.005
.004
.003
.008
0
.003
0
0
0
.001
0
0
31
11
9
2
1
1
0
0
0
0
1
0
.041
.015
.012
.003
.001
.001
0
0
0
0
.001
0
13
40
15
4
2
1
0
3
0
0
0
0
.015
.046
.017
.005
.002
.001
0
.003
0
0
0
0
6
7
7
2
3
1
2
0
1
0
1
0
.008
.009
.009
.003
.004
.001
.003
0
.001
0
.001
0
24
5
15
0
0
0
1
0
1
0
0
0
.027
.006
.017
0
0
0
.001
0
.001
0
0
0
86
69
50
14
6
5
4
3
2
2
2
1
.018
.015
.011
.003
.001
.001
.001
.001
.0004
.0004
.0004
.0002
(Rhogeessa io) were captured in all sampling
periods (Tab. 2). In contrast, in Patı́a the
species richness was more variable, with the
lowest number of species observed in September (5 species) and the highest in June (9
species) (Tab. 3). In this area only A.
jamaicensis, C. perspicillata and Phyllostomus
discolor were captured in all sampling periods
(Tab. 3).
Species relative abundance
In Chicamocha, a total of 478 phyllostomid
bats were captured with mist-nets, while in
Patı́a 244 bats were captured with this
method. The relative abundance of phyllostomids was higher in Chicamocha than in
Patı́a (Tabs. 2 and 3), at every sampling
period except February, and this difference
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
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F. Sánchez et al.
Fig. 2. Rarefaction curves for the Phyllsotomidae in Chicamocha (lower solid line with dashed-line 95%
confidence interval) and in Patı́a (upper solid line with dash–dotted-line 95% confidence interval). The
confidence intervals of the curves overlap i.e., there is not significant difference between the observed species
richness of the two sites.
Table 4. Total species richness of Phyllostomidae for Chicamocha and Patı́a estimated with the non-parametric
estimators of Chao 1, Chao 2, incidence-based coverage (ICE), abundance-based coverage (ACE), Jackknife 1
(Jack 1), and Jackknife 2 (Jack 2). CI 95%=confidence interval 95%.
Chicamocha
Patı́a
Chao 1 CI 95%
Chao 2
Chao 2 CI 95%
ACE
ICE
Jack 1
Jack 2
11–11
12–12
11
12.24
11–11.01
12.01–16.68
11.57
12.35
11.45
13.08
11.97
13.95
12.91
13.07
was significant (Mann–Whitney U-test,
U=3.0, P=0.028).
Most of the captured individuals in Chicamocha belonged to the species G. longirostris
and S. lilium in all sampling periods, except
in April when A. lituratus was more abundant
than G. longirostris. The species A. lituratus,
A. jamaicensis, G. soricina, and R. io were at
an intermediate level of abundance. The
remaining species had relative abundance
values lower than 0.006 bats (net. hour)1
and, except for C. perspicillata, were absent
in at least one of the sampling periods (Tab.
2).
The most captured species in Patı́a, A.
jamaicensis, C. perspicillata and P. discolor,
were recorded at all sampling periods. All
other bat species had relative abundance
values lower than 0.003 bats (net. hour)1
and were not constant along the sampling
periods (Tab. 3).
Clear differences in the number of captures of
the species shared between Chicamocha and
Patı́a were detected. For example, S. lilium
was the most frequent species in Chicamocha, but was rarely captured in Patı́a. The
species C. perspicillata and P. discolor were
not frequent in Chicamocha but were relatively abundant in Patı́a.
Discussion
Species composition – The absence of
dry-forest dwelling bats in Patı́a
Dry zones increased in extent in the tropical
and subtropical areas of the New World
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
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Bats of two tropical dry forests of Colombia
during the Pleistocene because of the global
decrease in temperature and rainfall associated with glaciation (Haffer 1967; Pennington et al. 2000). In Colombia, existing dry
areas along the Caribbean coast expanded,
eventually connecting with dry areas of the
Magdalena River valley and forming a vast
dry region (Hernández-Camacho et al. 1992).
Sarmiento (1975) recognized a high affinity
of the floras from dry formations of northern
South America, and suggested that interAndean dry zones may have connected dry
areas of the Caribbean and those of the
coasts of Ecuador and Peru. However,
Hernández-Camacho et al. (1992) considered
that although there was an expansion of the
dry areas along the slopes of Cauca and Patı́a
valleys, probably there was no continuous
arid corridor that linked them with the
Caribbean dry zones because of a humid
barrier in what are today the departments of
Caldas and Risaralda in Colombia. These
two contrasting hypotheses lead to two
different predictions regarding the presence
of dry-zone dwelling bats in Patı́a. The
presence of arid-zone bats would be consistent with an extensive dry area along the
Cauca River basin that may have been
connected with dry areas in Ecuador and
Peru, while their absence would be consistent
with discontinuous dry areas along the Cauca
River basin.
Of particular interest for the testing of these
hypotheses is the distribution of G. longirostris and R. io, which have been reported
in dry areas of the Colombian Caribbean
lowlands and in the dry enclaves of the
Magdalena River valley (LaVal 1973; Genoways and Baker 1996). The species G. longirostris is also present in the northern
Venezuelan dry forests (Webster et al.
1998), while R. io is replaced along the
Atlantic coast by R. minutilla (Genoways
and Baker 1996). We did capture both G.
longirostris and R. io in Chicamocha, and did
not catch either species in Patı́a. It could be
argued that we did not record R. io in Patı́a
due to the method of capture (mist-nets).
However, mist-netting has been enough to
detect Rhogeessa species when they occur in
dry ecosystems, such as Chicamocha and
Lagunillas, Venezuela (Sosa et al. 1996).
7
The current distribution of G. longirostris and
R. io coincides with that of other mammals
such as Heteromys anomalus (Anderson 1999)
and Sigmodon hispidus (Voss 1992), which
occur in dry areas of the Caribbean lowlands
and Magdalena River basin, and are absent
in the valleys of the Cauca, Dagua and Patı́a
rivers. The distribution of these mammals
supports the hypothesis of a connection
between the Caribbean dry zones and the
upper Magdalena River dry areas, but not
between the Caribbean lowlands and the
Cauca and Patı́a dry forests during the
Pleistocene.
Nonetheless, the presence of the rodent
Zygodontomys brunneus, a dry-forest dwelling species, on the slopes of the upper Cauca
and Magdalena rivers (Voss 1991) partly
contradicts the above evidence. Thus, it is
still necessary to explore other dry enclaves
north of Patı́a in the Cauca River basin for
the presence of G. longirostris and R. io.
Species richness
According to Murphy and Lugo (1986),
tropical dry forests have mean annual rainfall
ranging from 250 to 2000 mm. Given that
increase of rainfall in dry ecosystems leads to
increase of productivity (Rosenzweig and
Abramsky 1993), we would expect to find
an increase in bat species richness along the
rainfall gradient in dry forests. Hence, one
could expect that Patı́a would have higher
species richness than Chicamocha, because
the former region receives more rainfall
during the year than Chicamocha. Our
results partially support this prediction. The
observed species richness of Phyllostomidae
is not significantly different between the two
sites, but the estimated total richness of
phyllostomids is higher in Patı́a than in
Chicamocha. This result is suggestive; however we are aware that the analysis of
additional assemblages from Neotropical
dry forests is needed before making a
generalization on the relationship between
productivity and phyllostomid species richness in this ecosystem.
With potentially more phyllostomid species
than Chicamocha, the Patı́a assemblage had
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
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F. Sánchez et al.
higher variability in number of species during
the sampling periods than Chicamocha. In
Chicamocha, five out of the 11 captured
phyllostomid species were present in all the
samplings. In contrast, nine of the 12 species
in Patı́a were not recorded during two or
more sampling periods. Tropical dry forests,
such as Chicamocha and Patı́a, have periods
of very low rainfall which may impose major
limitations for the growth and development
of plants (Murphy and Lugo 1986), and
consequently may affect the production of
plant products (e.g., fruit and flowers) and
arthropod populations. Therefore, it is possible that very mobile animals such as bats
would opt for moving away from the forest
during the driest periods, when resources such
as food may be limiting (Heithaus et al. 1975).
This idea is supported by the fact that the
lowest number of species captured in both
Chicamocha and Patı́a fell on the last months
of the driest season of the year (February and
September, respectively). The effect of rainfall
seasonality on the variability of number of
species in Patı́a may have also been augmented by the absence of dry-zone dwelling bat
species, such as G. longirostris, which is
present in Chicamocha during the entire year.
The high variability in the species composition and number of species in Patı́a may also
be related to the abundance of bats in this dry
zone.
Species relative abundance
Assuming that capture success is related to
abundance of phyllostomids in the study
areas, Patı́a had a significantly lower abundance of these bats compared to Chicamocha. This result disagrees with what could be
expected from the relationship between
abundance and productivity in dry ecosystems, i.e., the higher the productivity the
larger the population sizes (Rosenzweig and
Abramsky 1993). Thus, although our results
on the richness of phyllostomids appear to fit
the expected pattern related to productivity,
our results on the abundance of phyllostomids did not. We propose that this discrepancy may be due to the effect of human
disturbance in Patı́a. In this region, humans
have indiscriminately persecuted bats since
they regard them all as ‘‘vampire bats’’; in
addition, this zone has suffered from severe
fragmentation and destruction of the natural
habitats (Gast et al. 1997). These two factors
may explain, at least partially, the low
capture frequency of bats in Patı́a.
Bat–columnar cactus interactions and bat
assemblage structure
In the dry forests of northern South America
such as Chicamocha, Tatacoa (Colombia) and
Lagunillas (Venezuela) a close plant–animal
relationship has been developed between
Glossophaginae bats and columnar cacti
(Soriano et al. 1991; Ruiz et al. 1997; Cadena
et al. 1998; Soriano et al. 2000). In this
interaction, the bat benefits nutritionally by
consuming both fruit and nectar-pollen, and
the cactus takes advantage of the pollination
and seed dispersal services of the bat.
In Chicamocha, the two most abundant species
include an important proportion of columnar
cacti resources in their diet. Glossophaga longirostris includes both fruit and nectar-pollen,
while S. lilium includes fruit and minor
amounts of nectar-pollen of these plants
(Cadena et al., unpublished results). Although
in Patı́a there are two species of Glossophaginae, Anoura geoffroyi and Choeroniscus godmani, none of them has a close interaction with
columnar cacti. In this zone, several phyllostomids exploit flowers and fruit of these plants,
but no species specializes in their consumption.
Nevertheless, even though P. discolor behaves
as an eclectic plant eater (sensu Giannini and
Kalko 2004), it may be one of the most
important pollinators of the columnar cacti in
Patı́a given its abundance and the high
frequency of its visits to the flowers of these
plants (Alvarez, unpublished data). The fruits
of the two most common columnar cacti of the
zone, Pilosocereus sp. and S. griseus, form a
considerable part of the diet throughout the
year for three species of bats, A. jamaicensis, C.
perspicillata and P. discolor (Alvarez, unpublished data). Thus, phyllostomids bats may
play an important role in the sexual reproduction of columnar cacti in Patı́a.
Cadena et al. (1998) suggested that the high
abundance of G. longirostris and S. lilium in
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
ARTICLE IN PRESS
Bats of two tropical dry forests of Colombia
the Chicamocha region is favored by their
capability to exploit the resources offered by
columnar cacti. This hypothesis is
supported by the results from Patı́a, because
the three dominant species are the main
consumers of the fruits and/or flowers
of columnar cacti. Furthermore, in Tatacoa
G. longirostris and C. perspicillata, the two
most abundant species in the area, include
considerable amounts of columnar cacti fruit
in their diet (Ruiz et al. 1997). Hence, the
capability of using the resources offered by
columnar cacti appears to affect the structure
of the bat assemblages in Neotropical dry
forests where columnar cacti are abundant.
We also found that some bat species regarded
as specialists in non-cacti fruit types, e.g.,
Carollia in Piper spp., Sturnira in Solanum
spp., and Artibeus in Ficus spp. (Cloutier and
Thomas 1992; Giannini 1999; Giannini and
Kalko 2004), may include fruit of columnar
cacti as an important part of their diet in dry
ecosystems, which reflects the flexibility of
these species regarding diet selection.
Finally, if plans for the conservation of bats
and their environment are going to be
implemented either in Chicamocha or Patı́a,
the link between bats and columnar cacti
need to be considered. In addition, we cannot
forget that bats obtain resources not only
9
from the xerophytic vegetation, but also from
the riverine habitats (Cadena et al. 1998).
Hence, modifications in the landscape of
tropical dry forests could have important
effects on the dynamics of bat communities.
Acknowledgements
We would like to thank the botanists of the
Herbario Nacional Colombiano for their
collaboration in the identification of plant
samples. Thanks also to Adriana Albesiano
for her assistance during the fieldwork
and in the determination of plant samples,
to Miguel Rodrı́guez and Marcela
Gómez-Laverde for their collaboration in
the examination of the specimens of
Rhogeessa and Micronycteris in the collection
of the ICN, to Yaneth Muñoz curator of the
mammal collection of the ICN, and to an
anonymous reviewer for translation of the
abstract into German. Claudia E. Moreno,
Robert P. Anderson, Rimma Gluhih, Pascual
Soriano, Micha" Wojciechowski, Chris Tracy, Dinesh Rao, Dieter Kruska and one
anonymous reviewer provided comments and
suggestions for improving the manuscript.
This research was supported by COLCIENCIAS, project code 1101-13-011-93.
Zusammenfassung
Struktur von Fledermausgemeinschaften in zwei Trockenwäldern Kolumbiens: Zusammensetzung, Artenreichtum und relative Häufigkeit
Wir untersuchten die Zusammensetzung, den Artenreichtum und die relative Häufigkeit von
Fledermausgemeinschaften in den Trockenwäldern von Chicamocha und Patı́a in Kolumbien. In
Chicamocha wurden 13 Arten (11 davon Phyllostomidae) mit Japannetzen gefangen. Dies entsprach
85–100% der für dieses Gebiet geschätzten Artenzahl. In Patı́a hingegen wurden 12 Arten mit
Japannetzen gefangen, alle davon waren Phyllostomiden. Dies entsprach 72–100% der für dieses
Gebiet geschätzten Artenzahl. Die Gemeinschaftsstruktur in Chicamocha unterschied sich nur
geringfügig in Artenreichtum und Zusammensetzung über die Zeit. Die häufigsten Arten in diesem
Trockenwald waren Glossophaga longirostris und Sturnira lilium. In Patı́a hingegen fanden wir
deutliche Unterschiede in der Artenzusammensetzung über die Zeit. Die häufigsten Arten waren dort
Artibeus jamaicensis, Carollia perspicillata und Phyllostomus discolor. Typische Trockengebietsarten
waren in Patı́a nicht vertreten. Wir nehmen an, dass das Fehlen dieser Arten mit der Isolierung
Patı́as von den anderen, nördlich gelegenen Trockenzonen Kolumbiens seit dem Quartär
zusammenhängt. Die Fledermausgemeinschaft in Patı́a war auch durch niedrigere relative
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003
ARTICLE IN PRESS
10
F. Sánchez et al.
Häufigkeiten und geringerer Stabilität in der Artenzusammensetzung charakterisiert. Dies ist
vermutlich in Zusammenhang mit Störungen zu sehen, die von Menschen verursacht werden. Die
häufigsten Phyllostomiden-Arten in den beiden untersuchten Trockenwäldern wiesen Früchte
und/oder Nektar und Pollen von Säulenkakteen als wichtige Nahrungsbestandteile auf.
r 2006 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
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Authors’ addresses:
Francisco Sánchez, Mitrani Department of Desert
Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990
Midreshet Ben-Gurion, Israel Jimmy Alvarez, Departamento de Biologı́a, Universidad Nacional de Colombia, Ciudad Universitaria, edificio 421, Bogotá,
Clara Ariza, Plant Ecology Department, University of
Tuebingen, Auf de Morgenstelle 3, Tuebingen, 72076,
Germany Alberto Cadena, Instituto de Ciencias
Naturales, Universidad Nacional de Colombia, P.O.
Box 7495, Bogotá, Colombia
(e-mail: fasbos@gmail.com
Please cite this article as: F. Sánchez et al., Bat assemblage structure in two dry forests of Colombia:
Composition, species..., Mamm. biol. (2006), doi:10.1016/j.mambio.2006.08.003